Georgia State University Digital Archive @ GSU
Anthropology Theses Department of Anthropology
4-24-2007 Taxon, Site and Temporal Differentiation Using Dental Microwear in the Southern African Papionins Darby Proctor [email protected]
Recommended Citation Proctor, Darby, "Taxon, Site and Temporal Differentiation Using Dental Microwear in the Southern African Papionins" (2007). Anthropology Theses. Paper 21. http://digitalarchive.gsu.edu/anthro_theses/21
This Thesis is brought to you for free and open access by the Department of Anthropology at Digital Archive @ GSU. It has been accepted for inclusion in Anthropology Theses by an authorized administrator of Digital Archive @ GSU. For more information, please contact [email protected]. TAXON, SITE AND TEMPORAL DIFFERENTIATION USING DENTAL
MICROWEAR IN THE SOUTHERN AFRICAN PAPIONINS
By
DARBY PROCTOR
Under the Direction of Frank L’Engle Williams
ABSTRACT
The evolutionary history of the South African papionins is a useful analog for the emergence of hominids in South Africa. However, the taxonomic relationships of the papionins are unclear. This study uses low-magnification stereomicroscopy to examine dental microwear and uses the microwear signals to explore the existing classification of these papionins. The results from the species and site level analyses are equivocal.
However, the genera and time period results show clear evidence for a dietary change between the extinct and extant forms of Papio and Parapapio. This adds an additional tool for distinguishing these two groups. The dietary changes witnessed in the papionins are likely found in the hominids from the Plio-Pleistocene. Using the papionin analog, hominid dietary evolution may be explored.
INDEX WORDS: Papionins, South Africa, Plio-Pleistocene, Dental microwear,
Hominids, Papio, Parapapio
TAXON, SITE AND TEMPORAL DIFFERENTIATION USING DENTAL
MICROWEAR IN THE SOUTHERN AFRICAN PAPIONINS
by
DARBY PROCTOR
A Thesis Submitted in Partial Fulfillment of Requirements for the Degree of
Masters of Arts
in the College of Arts and Sciences
Georgia State University
2007
Copyright by Darby Proctor 2007
TAXON, SITE AND TEMPORAL DIFFERENTIATION USING DENTAL
MICROWEAR IN THE SOUTHERN AFRICAN PAPIONINS
by
DARBY PROCTOR
Major Professor: Frank L. Williams Committee: Susan McCombie Cassandra White
Electronic Version Approved
Office of Graduate Studies College of Arts and Sciences Georgia State University May 2007 iv
ACKNOWLEDGEMENTS
This project would not have been possible without the support of many people, all of whom I am indebted to. I would like to thank my advisor, Frank Williams, for providing Georgia State with an exceptional collection of primate dental casts as well as guiding me through this process. I also want to thank my committee members, Susan
McCombie and Cassandra White, for their guidance and support as well as for reading this esoteric, even by anthropology standards, thesis.
Christopher Watt provided me with invaluable help with my bibliography as I was starting this project. Nev Ertas helped me with some statistical quagmires and saved my sample size. Thank you.
I would also like to thank my parents, Cort and Lona Proctor, who have always supported education and who have to listen to me talk about primates more than they
probably care to. Finally, I want to thank Molly Larson, who devoted many hours to
helping me with revisions and more importantly, provided me with the emotional support
necessary get through writing this thesis.
v
TABLE OF CONTENTS
ACKNOWLEDGEMENTS…………………………………………………….. iv
LIST OF TABLES……………………………………………………………… vi
LIST OF FIGURES…………………………………………………………….. vii
LIST OF ABBREVIATIONS…………………………………………………... viii
CHAPTER ONE: INTRODUCTION…………………………………………... 1 Past Research……………………………………………………. 2
CHAPTER TWO: THE CONTEXT FOR THIS STUDY……………………… 8 Papionin Relationships and Evolution…………………………... 8 Sites……………………………………………………………… 10 Climate Change and Evolutionary Theories…………………….. 12 History of Dental Microwear……………………………………. 16
CHAPTER THREE: MATERIALS AND METHOD………………………….. 21 SEM, SCM and LMS……………………………………………. 21 Microwear and Species Differentiation…………………………. 24 Materials…………………………………………………………. 25 Method…………………………………………………………... 27 Statistical Analyses……………………………………………… 28
CHAPTER FOUR: RESULTS………………………………………...……….. 32 Results by Species……………………………………………….. 32 Results by Genera…….…………………………………………. 38 Results by Site…..………………………………………………. 42 Results by Time Period………………………………………….. 47
CHAPTER FIVE: DISCUSSION AND CONCLUSIONS……………...... 53 Discussion……………………………………………………….. 53 Conclusions……………………………………………………… 58
REFERENCES…………………………………………………………...... 61
APPENDIX…………………………………………………………………...... 74 Specimens by Species…………………………………………… 74 Specimens by Site……………………………………………….. 79 vi
LIST OF TABLES
1 Reassigned Specimens 27
2 Mean and Standard Deviation of Microwear Features by Species 34
3 ANOVA Results for Species 34
4 Significant Results from Tukey’s HSD by Species 35
5 PCA Component Loadings by Species 36
6 DFA Classification Results by Species 38
7 ANOVA Results by Genera 40
8 PCA Component Loadings by Genera 41
9 DFA Classification Results by Genera 42
10 Sample Size by Site 43
11 ANOVA Results by Site 45
12 Significant Results from Tukey’s HSD by Site 45
13 DFA Classification Results by Site 47
14 ANOVA Results by Time Period 50
15 PCA Component Loadings by Time Period 51
16 DFA Classification Results by Time Period 52
vii
LIST OF FIGURES
1 Bivariate Graph of Total Pits and Scratches by Species 32
2 Graph of PCA Axes 1 and 2 by Species 37
3 Bivariate Graph of Total Pits and Scratches by Genera 39
4 Graph of PCA Axes 1 and 2 by Genera 41
5 Bivariate Graph of Total Pits and Scratches by Site 44
6 Graph of PCA Axes 1 and 2 by Site 46
7 Bivariate Graph of Total Pits and Scratches by Time Period 49
8 Graph of PCA Axes 1 and 2 by Time Period 51
viii
LIST OF ABBREVIATIONS
ANOVA Analysis of Variance
DFA Discriminant Function Analysis
DNA Deoxyribonucleic Acid
HSD Honestly Significant Differences
LMS Low-magnification Stereomicroscopy
MYA Million Years Ago
PCA Principal Components Analysis
PSC Phylogenetic Species Concept
SCM Scanning Confocal Microscopy
SEM Scanning Electron Microscopy
1
Chapter One: Introduction
Monkeys, and specifically baboons, have long been linked to humanity from
recent television commercials depicting primates in cubicles, to medieval European
portrayals of devil monkeys (Schrader, 1986) and to the sacred status of baboons in
ancient Egyptian mythology (Carter and Carter, 1999). The link between baboons and
humans goes even further than recorded histories and into their common evolutionary
past. Both papionins and hominids were evolving in southern Africa during the Plio-
Pleistocene epoch (Jablonski, 2002; Jolly, 2001). Jolly (2001) argues that because of this
shared past, in terms of time, geography, and complexity of the species relationships
within these groups, the papionins can be useful as analogies to hominid evolution.
However, the extinct southern African Plio-Pleistocene papionins are poorly understood in terms of their species designations as are the extant baboons, although the extant baboons are becoming more well understood due to genetic studies (Newman et al., 2003). A variety of methods have been used in previous studies to explore the relationships among the papionins. However, there is still much confusion. Therefore, this study applies the novel method of low-magnification stereomicroscopy (LMS) to the poorly agreed upon species designations in the southern African papionins which extends
from the Plio-Pleistocene to the present. Specifically, two genera of baboon-like forms
will be investigated: Parapapio from southern Africa during the Plio-Pleistocene, extinct
Papio from Southern Africa during the Plio-Pleistocene, and extant Papio from across
Africa. Parapapio is a generalized baboon form that may be ancestral to modern living 2
baboons, although that relationship is still unclear (Disotell, 1994; Groves, 2000; Jolly,
1967; Jolly, 1970b; Szalay and Delson, 1979; Williams et al., 2007). The genus Papio is
somewhat better understood since many species are extant. However, extinct forms such
as Papio izodi are also addressed here.
Past Research
The literature on these two genera in regards to species differentiation is
equivocal with few authors agreeing on what characteristics define each taxon and which
specimens belong to which species (Benefit, 1990; Broom, 1940; Delson, 1975; Disotell,
1994; Disotell, 1996; El-Zaatari et al., 2005; Freedman, 1957; Freedman, 1960;
Freedman, 1961; Freedman, 1965; Freedman, 1976; Freedman and Stenhouse, 1972;
Gear, 1926; Jablonski, 2002; Jolly, 2006; Maier, 1970; Maier, 1971; Proctor and Hudson,
2006; Simons and Delson, 1978; Williams et al., 2006). The debate over species
designations is two-fold. In large part, the debate is due to the lack consensus over which
species concept to use in the fossil record. Second, there is no methodological agreement
for how to categorize the specimens.
One example of the equivocation in the field is evidenced by the work of
Freedman (1976) and Maier (1970). Both examined the same specimens (M.3051,
M.3060 and M.3061 from Makapansgat) and arrived at different species designations
within the genus Parapapio. Their designations were based on interpretations of species-
specific characteristics. Freedman (1976; pg. 303) notes that having “three
morphologically very similar species [of Parapapio]…always appeared disturbing.” The
three species he is referring to, Pp. broomi, Pp. jonesi, and Pp. whitei, appear to be scaled
versions of each other. That is, the three species of Parapapio, are morphologically 3
similar, except in their size. Yet, the sizes of the three species all overlap. The varying sizes would be logical if there were a chronological progression or even a significant geographic variation, but they co-occur in the same Pliocene-dated sites (Makapansgat,
Sterkfontein and Taung). This suggests that either these size differences may not be indicative of individual species or that the sites have significant temporal depth.
Freedman’s (1957, 1960, 1961, 1965; Freedman and Stenhouse 1972) classification of Parapapio is largely based on the dimensions of the second and third molars although measurements of the canines, premolars and first molar are occasionally reported (Freedman, 1965). This method has problems. In one instance, Freedman (1960) discusses several specimens that he identifies as belonging to Parapapio but cannot identify the species because the molars are missing even though the cranium is largely complete. Freedman (1960) notes that some specimens seem to overlap to which species they could be assigned based on molar dimensions. This lack of agreement and the resulting presence of three scaled species suggests that the species designations may not be accurate. Additionally, Freedman (1960) cites another paper (Leakey and Whitworth,
1958) that states that size differences are not enough to warrant separate species. Even though this paper was written about a different primate genus, Simopithecus, it highlights the difficulty of declaring species based solely on the size of cranial remains.
In a later paper Freedman (1965), extends the range of variation in molar dimensions that is permissible in another species, Papio robinsoni, despite being unable to find differences between the molar dimensions of P. robinsoni, which is a Plio-
Pleistocene baboon form and P. ursinus, which is extant. In other words, a relatively well-understood living baboon, P. ursinus, has less variation in molar dimensions 4
between individuals than does the extinct P. robinsoni. This makes using molar
dimensions to distinguish species suspect. Furthermore, the variation in molar
dimensions of each of the three co-occurring Parapapio forms is greater than the
variation found in the extant Papio ursinus (Freedman and Stenhouse, 1972). This again
suggests that the original methods used to classify these species could not capture
distinctions between taxa.
Interestingly, Freedman, whose work is often cited for species designations in
Parapapio, could not decide how to classify some specimens. First, Freedman (1957) classified a particular specimen from Taung (56604) as Parapapio antiquus. Then he decided it was P. wellsi (1961) and ultimately decided that it is indeed Pp. antiquus
(Freedman, 1965). Pp. antiquus is a species from Taung that is often described in its similarity to P. wellsi and P. izodi (Freedman, 1961). If Pp. antiquus is so elusive to classify and it bears striking similarities to P. wellsi and P. izodi, these species may not be real biological units. Clearly this specimen, and perhaps all specimens grouped as Pp. antiquus, needs to be reexamined in order to verify the species designations.
Adding to the confusion in the literature about these species is the absence of a consensus on which species concept to use as a reference. Living species are often classified based on soft tissue and behavioral differences. Since all fossil remains consist of hard parts (crania, teeth, etc.) and behaviors cannot be observed, the phylogenetic species concept (PSC) seems most applicable (Groves, 2004). Groves (2004; pg. 1110) defines the PSC as “the smallest cluster of individual organisms within which there is a parental pattern of ancestry and descent and that is diagnosably distinct from other such clusters by a unique combination of fixed character states.” This is to say a species is 5
made up of the smallest group of individuals that all have common traits that differ from
other similar animals.
In this study, dental microwear will be used as the fixed character state, or trait
with the acknowledgement that dental microwear is not fixed. However, due to the lack
of agreement in the literature based on fixed states (i.e. molar size), dental microwear will
be explored as a theoretical fixed state. Groves (2004, pg. 1110) continues, “ a species
has one or more fixed differences from other species; it is 100% different; so one asks not
how much difference is necessary to decide whether a population rates as a species, but
what proportion of individuals differ? Any kind of character will suffice, be it color, size,
vocalization, or a DNA sequence, as long as there is a reasonable supposition that the
difference is heritable.” It is interesting to note that size is listed as one possible
distinguishing feature of a species. However, in the three Parapapio species, there is not
a 100% difference between the sizes of the species. The three southern African forms of
Parapapio all overlap in their size ranges. This makes size not a valid argument for
different species under the PSC in the context of Parapapio.
In this study, it is acknowledged that microwear is not heritable, but the patterns
that produce microwear (i.e. the cranial and dental morphologies which correspond to diet) are heritable. Diet, as indicated by various features of teeth, is frequently used in the primate fossil record to infer behavior (Kay et al., 2004; Ungar, 1999; Wolpoff, 1973).
Microwear can then be used as a proxy for the requirements of determining species differentiation based on the phylogenetic species concept.
Godfrey and Marks (1991) agree that the phylogenetic species concept is often the only species concept that can be applied to the fossil record. An important caveat that 6
Godfrey and Marks (1991) note is that there should be no more variation in a fossil
species than what is found in their closest living relative. For example, a rough range of
the size of third molars can be established for a relatively well-understood living baboon
species. That range could then be compared to the range in a fossil baboon species. If the
range is either significantly greater or less than the living baboon range, this suggests that
the fossil species is not well defined.
However, species concepts in living primates can be just as complex. This is
especially true of the papionins, who have natural hybrid zones in the wild (Godfrey and
Marks, 1991). Because of these natural hybrid zones, many of the species concepts are
difficult to apply to the papionins. The extant papionins are often geographically
separated, yet interbreeding occurs when they come into contact in the wild and in
captivity. The result is that there are varying opinions on how the closely related baboon
groups should be classified. This is further complicated by the natural hybrid zone in
which Papio hybridizes with Theropithecus, who diverged from the Papio lineage some
3.75 million years ago (mya) while the remaining baboons had a common ancestor
around 1.75 mya (Newman et al., 2003). It is interesting to note that if these two genera
that are closely related, but diverged over three million years ago can interbreed, it is
likely that the varying species of early hominids could have also interbred (Jolly, 2001).
If early species of Homo could have interbreed, some Plio-Pleistocene taxonomic
designation have little biological value (Scholz et al., 2000).
This study attempts to shed light on these complex genera, Parapapio and Papio by using dental microwear to 1) determine if the species designations that are assigned to specimens within the genera are statistically real groups, 2) determine what traits of the 7
microwear differentiate species (if any), 3) determine if there are redundant species labels, 4) determine if Papio and Parapapio can be distinguished using dental microwear and 5) explore the data to see if there are site or temporal differences among the specimens.
By determining if microwear can differentiate these species, an additional tool will be available to researchers dealing with the complex relationships among fossil primates. Additionally, the temporal variation in papionin diet may be examined and used as a vehicle to explore hominid evolution in Southern Africa because the evolution of
Papio and Homo occurred in the same time period and ecogeographic location. Papio and
Homo are also both encephalized compared to other mammals and are both dietary generalists/opportunists. The rapid dietary shifts in the papionins likely reflects habitat changes caused by climate fluctuations during the Plio-Pleistocene. Therefore, hominid food sources would likely shift just as papionin food sources changed. Thus, the southern
African papionins are important to understand in terms of the evolution of cercopithecids, but can also be an important tool for inferring habitat change that affected the Plio-
Pleistocene hominids.
8
Chapter Two: The Context for this Study
In order to fully grasp the complexity of the papionins, a brief introduction to the family Cercopithecidae, and specifically to the papionins, will be given. The evolution of the papionin lineage and the taxonomic relationships of the papionins is also of interest.
This is followed by a discussion of the sites at which this study’s materials were discovered. The site contexts are important due to their often close proximity to hominid remains. The evolution of papionins and hominids were heavily impacted by Plio-
Pleistocene climate change (Vrba 1983, 1993, 1996). Therefore, the climactic and evolutionary theories that are relevant to this region are discussed. Finally, a history of dental microwear is given in order to contrast low-magnification stereomicroscopy with more established methods.
Papionin Relationships and Evolution
The papionins are part of the family Cercopithecidae, otherwise known as the Old
World monkeys. The family Cercopithecidae is divided into two subfamilies, the
Colobinae, or the leaf eating monkeys, and the Cercopithecinae, which includes Papio and Parapapio, as well as macaques, guenons, geladas, and other species.
As a subfamily, the Cercopithecinae are relatively homogeneous. There is variation to be sure, but not to the extent that is found in other families. Cercopithecinae includes the most widespread primate genus, Macaca, which ranges in northwest Africa, across Asia and even into Japan, and the genus Papio.
9
The genus Papio, while not as widespread as the macaque group, is a successful
taxon that ranges throughout Africa. The distribution of Papio can be seen as a model for
the evolution of Homo in Africa, since Homo emerged in the same places at the same time as Papio. The Cercopithecinae tend to be more terrestrial than other groupings of monkeys, which has interesting implications for dental microwear and hominid evolution.
Since these groups, specifically the papionins, rely primarily on ground-based or low- hanging food resources their diet may contain more grit than that of arboreal species.
That is, terrestrial species tend to consume more sand and non-food particles than
arboreal species. The grit in the diet of terrestrial species leads to different patterns of
dental microwear than arboreal species.
Papio is the genus that contains all of the living baboons as well as several extinct
species. Hominids have been living sympatrically with baboons throughout the fossil
record. The oldest hominid remains are typically found in sites that also contain baboon
remains (McKee et al., 1995). For example, the Taung child, one of the most famous
Australopithecus fossils was found at a site that is also known for having deposits of
Papio and Parapapio (Freedman, 1961; Laitman, 1986). The term Papio was first used in
the scientific literature to identify living baboons by Müller in 1773 (Jablonski, 2002). In
contrast, Parapapio, the genus that includes fossil baboon forms that are closer to the ancestral form of all the papionins, has a much more recent history in the literature.
Parapapio was first named by Jones in 1937 (Jablonski, 2002; Jones, 1937). Parapapio
and Papio continue to be confused during the recovery of fossil remains, due to the
striking similarities between the forms. Parapapio tends to be smaller, and overlaps into
the range of the smaller Papio taxa. The feature that is most distinguishable between the 10
two is the slope of the muzzle, which can be difficult to ascertain depending on the state
of the fossil when it is retrieved and which portions of the crania, if any, are recovered
(Jablonski 2002). Despite the similarities, there is agreement in the literature that Papio and Parapapio should be maintained as two distinct genera (Jablonski, 2002; Szalay and
Delson, 1979).
Extinct and extant Papio are known from sites across sub-Saharan Africa.
Parapapio is primarily known from South Africa, but is also found in East and North
African early Pliocene through early Pleistocene deposits (Frost and Delson, 2002;
Jablonski, 2002; Szalay and Delson, 1979). The fossil specimens in this study all come from southern African locations but the extant forms range from across Africa. (See
Appendix for list of specimens and locations).
Sites
The materials for this study are primarily from the southern African cave sites of
Bolt’s Farm, Cooper’s Cave, Kromdraai, Makapansgat, Sterkfontein, Swartkrans and
Taung. However, comparative material from extant species was also used and grouped into the regional sites of South Africa (P. ursinus), Central Africa (P. kindae) and East-
Central Africa (P. anubis). See Appendix for the locations at which materials were acquired.
The sites of Bolt’s Farm, Cooper’s Cave, Kromdraai, Sterkfontein and Swartkrans are all found in the Sterkfontein Valley of southern Africa, which is located near the city of Krugersdorp, just west of the capital of Johannesburg. Makapansgat is located further
to the north near the city of Potgietersrust. Taung is southwest of Johannesburg, south of
the city of Vryburg. 11
The chronology of the southern African cave sites is very difficult to ascertain due
to the complex geologic history. This convoluted history has resulted in lack of a clear
stratigraphy for which to date the sites (Brain, 1981; Williams et al., 2007). As a result,
inferential comparative dating methods must be used to place these sites in temporal
context. First, an examination of faunal remains at these sites can be compared to similar
faunal remains in East Africa, where there is well-dated stratigraphy. Second,
biochronology, or relative dating based on the specimens found within the site, can be
established.
Vrba (1975) examines faunal (antelope) remains to date the sites of Sterkfontein,
Swartkrans and Kromdraai. Vrba (1975) finds Sterkfontein to be the oldest site having
remains that are dated to 2.5 to 1.6 million years ago (mya). Swartkrans Member 1 is
dated from 1.7 to 1.0 mya, while Swartkrans Member 2 is dated to be much more recent,
from 500,000 years ago. Kromdraai A dates from 1.3 to 0.7 mya, with Kromdraai B
dating from 0.7 to 0.2 mya. Vrba’s (1975) dating has been refined in more recent
publications. Based on U-Pb chronometry Swartkrans Member 1 has been dated to 2
mya, Member 2 to 2.02 to 1.44 mya and Member 3 to 0.988 mya (Albarede et al., 2006).
In more recent publications, these estimates have been refined by using
biochronology (Delson, 1984). Delson (1984) dates Kromdraai A and Swartkrans
Member 1 to 1.5 mya, Bolt’s Farm and Taung to 2 mya, Sterkfontein Member 4 to 2.5
mya and Makapansgat Member 3-4 to 3.0 mya. Another study (Williams et al., 2007)
examines papionin remains in the South African cave sites to determine their age.
Williams and colleagues (2007) state that Sterkfontein may bridge the Plio-Pleistocene boundary due to the presence of certain papionins. Similarly they suggest that 12
Makapansgat may also have extended from the middle Pliocene into the early
Pleistocene.
The dating of these sites is an important issue to be addressed because it plays a central role in understanding the evolution of both the papionins and hominids. A clear chronology must be established in order to theorize about possible extinction and speciation events. Additionally, some chronology must be established to understand the effect of climate change on both papionins and hominids.
Dental microwear may be able to help elucidate some of the dating problems. As dental microwear is evidence of diet, changes in dental microwear reflect changes in diet.
Thus, dietary reconstruction may be able to supplement other inferential methods such as faunal dating and biochronology.
Climate Change and Evolutionary Theories
It is widely agreed that the sites where Parapapio are found should be dated to the
Pliocene (Benefit, 1990; Benefit, 2000; Broom, 1940; Delson, 1975; Jablonski, 2002;
Szalay and Delson, 1979; Teaford and Leakey, 1992; Williams et al., 2007). There are two issues that make this time period particularly interesting. First, it is the time period in which some of the earliest hominids are found (Laitman, 1986; Leakey and Walker,
1997). Second, southern Africa, and most of the world, was experiencing a dramatic climate change during this period (Reed, 1997). Therefore, this climate change affected both the papionins that were living in southern Africa as well as the early hominids.
Theoretical models have been developed to account for the evolution and extinction events seen during this time period. 13
Several evolutionary theories that relate to reconstructing the evolution of
primates, as represented in the South African primate fossil record, are relevant. These
include Vrba’s turnover pulse (Vrba, 1983; Vrba, 1993; Vrba, 1996), Potts’ variability
selection hypothesis (Potts, 1998), Reed’s use of paleocommunity and taphonomy (Reed,
2002), as well as a variety of methods that relate more specifically to diet and dentition.
Vrba (Vrba, 1983; Vrba, 1993; Vrba, 1996) builds her turnover pulse hypothesis from the framework of punctuated equilibrium that was postulated by Eldredge and
Gould (1972). According to Vrba (1993), punctuated equilibrium implies that all species’ diversification is a result of physical environmental change. Vrba suggests, “if evolution within established species commonly produces net statis and if significant phenotypic change is associated with rare speciations, then what other special initiating cause
[emphasis from original] can be invoked but physical environmental change?” (Vrba
1993; pg. 427). Following this logic, all speciation and extinction events are a result of environmental change. Vrba goes on to conclude that Plio-Pleistocene South African evolutionary events are concentrated in a series of turnover pulses that stem from the cooling and drying of global climate change.
One of the strengths in Vrba’s (1993, 1996) argument is that the turnover pulse hypothesis can also work with phyletic gradualism. Under a gradualist theory, lineage splitting and extinction are rare events, which would require special explanation. The turnover pulse theory could serve to explain these rare events by using rapid climate change as the mechanism for the rare speciation events. Another factor that strongly supports the idea of a turnover pulse is the dramatic climate shift that occurred during the
Plio-Pleistocene as evidenced by ocean core samples (Denton, 1999) and the 14
corresponding speciation events that are seen in hominids and other primates during this
time (deMenocal, 1995; Reed, 1997).
The turnover pulse hypothesis posits that the physical environment, and the
species within it, stay static most of the time. However, periods of environmental change
and the corresponding changes in species adaptation and composition should be marked
by groups of pulses, or periods of rapid change (Vrba, 1993; Vrba, 1996). The
implication for fast dietary change on the part of primates is much the same here as it is
for punctuated equilibrium. Namely, adaptation to changing environmental conditions
must be rapid or extinction may occur.
In contrast to Vrba (1993, 1996), Potts suggests in his variability selection hypothesis that lengthy environmental changes over hundreds of thousands of years results in lineages of organisms facing multiple and substantial disparities in selective environments over time (Potts, 1998). The variability selection hypothesis, attempts to
explain the “evolutionary cause of versatility in longer intervals of more dramatic change
in an organism’s survival regime” (Potts, 1998). In other words, species will be more
successful if they can adapt to long-term pressures rather than adapting quickly to
dramatic events. This implies that species do not change their adaptations in response to one short-term environmental change as Vrba’s (1993, 1996) turnover pulse hypothesis suggests, but rather species adapt to a series of environmental fluctuations that occur over successive generations. Potts seems to suggest that turnover pulses occur, but that they are spread out over evolutionary time rather than being relatively concentrated. This theory is supported by the long-term climactic shifts, such as ice ages, that can be seen throughout the history of the Earth and the corresponding changes in flora and fauna 15
(Zachos et al., 2001). The implication for primate dietary adaptation is that over time, dietary adaptations shift as they respond to long-term environmental fluctuations.
Moving from broad evolutionary theory to other approaches, Reed (2002) presents a way to examine the evolutionary past through the use of paleocommunity, the study of ancient communities and ecosystems, and taphonomy, the study of what happens to remains after an animal dies. The purpose of tying paleocommunity and taphonomy together are to examine information from across time in context and examine ecological patterns that may have influenced primate behavior (Reed, 2002). That is, contextual evidence can supplement the morphological evidence from the fossil record in order to gain a more complete understanding of evolutionary pressures. Reed (2002) shows that each type of ecosystem (forest, desert, etc.) is occupied by different mammals in different locations, but the mammals fill a similar ecological niche regardless of the ecosystem.
Thus, most mammalian communities can be placed into varying ecological niches based on food availability and competition. The behavior of primates can be inferred based on the fact that individuals interact with the vegetation around them and influences the ecological outcomes of other mammalian species. When combined with morphological studies, the biological role of certain structures in fossil primates may be glimpsed. For example, many of the behavioral inferences made for extinct species are based on living analogues with similar ecological characteristics. Without a clear understanding of how a feature affects living primates, it is impossible to determine what behaviors would have been present in fossil primates.
An inherent problem in examining paleocommunities and taphonomy is the comparative method, which is understanding fossil forms through their extant relatives 16
(Reed, 2002). It can be difficult to ascertain the biological role of certain morphological
features of living primates even though behaviors can be observed. Without an extant
analogue for comparison, the comparative method can be problematic. Dental microwear
can be used in the context of the comparative method because living and extinct primate
use wear patterns can easily be compared.
History of Dental Microwear
Dental microwear arose out of the need to study primate diets in the fossil record.
It is well established that studying diet in living primates can give significant insight into
most aspects of primate behavior (Krebs and Davies, 1993). Since behavior cannot be observed directly in the fossil record, other methods must be used to infer diet and then infer behavior. Understanding diet in fossil primate forms helps to inform the evolution of dietary behaviors. Ecological change can also be inferred. Additionally, dental microwear provides an independent test on inferences of diet based on cusp form, such as
shearing crest length (Benefit, 2000).
In living primates, researchers can watch what primates eat and perform fecal
analysis to discover any food sources that their observations may have missed (McGrew
et al., 2005; Moreno-Black, 1978; Tutin and Fernandez, 2005; Williamson et al., 2005).
Since observations and fecal sampling are not an option for extinct and fossil primates,
diet has to be inferred using comparative methods (Ungar, 1998; Ungar, 2002). Using the
comparative method, anatomical features that relate to diet in living forms can be
examined and compared to fossil forms with the same features. If a trait is found to have
a particular function in living primates that have a diet type, it is hypothesized that the
trait in the fossil record would also indicate that diet. 17
Within the comparative method for examining diet in primates, there are two
broad approaches that can be used (Ungar, 2002): adaptive, or anatomical traits
(morphology) and measurements (allometry), and non-adaptive, or evidence that relates
to the actual foods that were eaten (see Ungar 2002).
The adaptive evidence can be divided into evidence from allometry and from
morphology. Allometry, or differences related to scaling, has been examined in regards to
broad dental allometry (Groves and Napier, 1968; Robinson, 1954), cheek tooth
allometry (Gould, 1971; Kay, 1975; Kay, 1978; Pilbeam and Gould, 1974), and incisor
allometry (Eaglen, 1986; Jolly, 1970a; Jolly, 1970b; Kay and Hylander, 1978). While
issues of scaling can be important in understanding broadly different primate diets, such
as insectivores and frugivores, it is not useful when comparing species with similar tooth
morphologies and similar diets. Additionally, broad dental allometry, that is macro
scaling comparisons, cannot reveal which teeth the selection pressures act upon.
Moreover, both cheek tooth and incisor allometry do not explain what is seen in living
primates without controlling for phylogenetic relationships, or how the species in
question are related (Ungar, 2002).
Fortunately, adaptive morphological evidence has been more successful than
allometric evidence for inferring diet in the fossil record (Ungar 2002). This includes
dental morphology (Crompton and Sita-Lumsden, 1970; Gregory, 1922; Kay, 1984;
Simpson, 1933), molar shearing quotient studies (Kay, 1978; Kay, 1984; Kay and Covert,
1984; Kay and Hylander, 1978), dental biomechanics (Lucas and Luke, 1984; Lucas et
al., 1994; Lucas and Teaford, 1994), enamel thickness (Kay, 1981; Simons, 1976; Simons
and Pilbeam, 1972), enamel structure (Maas, 1991; Maas, 1993; Maas, 1994; Maas and 18
O'Leary, 1996), and mandibular form (Greaves, 1988; Greaves, 1993; Hiiemae and Kay,
1972; Rosenberger, 1986). Each of these methods examines the underlying structures of
the dentition in order to determine which foods were the focus of the diet and how those
structures and diets evolved (Ungar 2002). However, they must often be used in
conjunction with other measures such as body size to arrive at any correlations with
living primates (Kay, 1984). Additionally, these methods often require fossil specimens
that are more complete, as in using mandibular form, or require some invasive techniques
as in using enamel structure and enamel thickness. These requirements often make these
methods unsuitable for fossil specimens due to their rarity and incomplete nature.
There are fewer non-adaptive signals for diet in the primate fossil record. The main non-adaptive signals include tissue analyses, such as stable isotope (Ambrose and
DeNiro, 1986; DeNiro and Epstein, 1981) and trace element analysis (Lee-Thorp et al.,
1994; Sillen, 1992), and tooth wear analysis both on a macro (Meikle, 1977; Teaford,
1982) and micro (Rensberger, 1978; Walker et al., 1978; Walker, 1976) level. Tissue analyses can be quite difficult with fossils. This is due to lack of adequate samples as well as the difficulty in predicting the environment based on these ratios and elements.
This is largely because different environments can have the same results in the analyses
(Ungar 2002). Macro tooth wear may prove useful if calibrated to living analogs.
However few scientists are actively using this method.
Dental microwear, which examines the use wear patterns on teeth at a microscopic level, eliminates many of the problems evidenced in the above methods.
First, since dental microwear is based solely on the marks left behind by broader dietary strategies (i.e. frugivory, folivory, etc.), there is no need to account for allometric 19
differences in most comparisons (Godfrey et al., 2004). Second, there is little difficulty comparing across regions and time because the broader dietary categories apply throughout space and history. For example, a frugivorous primate from the Pliocene would have similar microwear patterns to a living frugivore. This is largely because the structure of fruit has not changed over time (Barlow, 2000). Since the structure of food sources has not changed, living and extinct diets can be reliably compared using dental microwear.
As a result, dental microwear is useful in tracking the dietary changes of a species through time. This can shed light into both how the species evolved and how the environment influenced those changes. In the southern African papionins and hominids, changes in dental microwear may reflect the changing climate during the Plio-Pleistocene and demonstrate how these species coped with altering food availability by changing their diets. This may also tie into discussions of extinction and speciation events, such as
Vrba’s (1983, 1993, 1996) turnover pulse by demonstrating an ecological factor that may have resulted in these events.
Additionally, the taxonomy of the papionins may be clarified by reexamining the existing species designations through dental microwear. Changing dietary signals may provide a chronology of the papionins centering around the Plio-Plesitocene climate shift.
Dental microwear may also help differentiate species that lived sympatrically because sympatric species typically occupy slightly different food niches (Harcourt, 1998; Milton,
1981; Porter, 2001; Tutin and Fernandez, 2005).
Ungar (2002) thoroughly reviews dental microwear methods using scanning electron microscopy (SEM). However, he does not address the newer methods of 20
scanning confocal microscopy (SCM) (Scott et al., 2005; Ungar et al., 2003) nor low- magnification microscopy (LMS) (Godfrey et al., 2004; Semprebon et al., 2004). Since dental microwear is of the most interest here, these three methods of inferring diet will be examined at length.
21
Chapter Three: Method and Materials
SEM, SCM and LMS
Dental microwear examines the microscopic pits and scratches that are left in the
occlusal surface of teeth as food is processed. These data are used to infer diet. Different
foods, such as nuts and leaves, will leave measurably different microwear on the tooth
surface. The first attempt at using dental microwear was made by Philip Walker (Walker,
1976). He used a light microscope to examine the striations on the incisors of Colobinae
and Cercopithecinae and an external light source to highlight striations that were not
visible under direct observation. He found that the orientation of the striations differed between these two groups. While his study had the possibility of becoming the seminal work in dental microwear, that honor fell to a different Walker (Walker et al., 1978) and
Rensberger (1978), just two years later.
In these seminal works (Rensberger, 1978; Walker et al., 1978), a scanning electron microscope (SEM) was first applied to the examination of dental microwear.
Since then the SEM technique of examining dental microwear has become the standard, with numerous studies using the method (Covert and Kay, 1981; Daegling and Grine,
1999; El-Zaatari et al., 2005; Gordon, 1982; Gordon, 1983; Gordon, 1984; Gordon, 1988;
Kay and Covert, 1983; Maas, 1991; Teaford, 1985; Teaford, 1988; Teaford, 1993;
Teaford, 1994; Teaford and Leakey, 1992; Teaford and Robinson, 1989; Teaford and
Walker, 1984; Ungar, 1996; Ungar et al., 1995).
22
In an effort to explain the techniques employed in using SEM to examine dental
microwear, the methods of a recent study by El-Zaatari and colleagues (El-Zaatari et al.,
2005) will be summarized here. First, the fossil specimens are cleaned with either acetone
or ethyl alcohol. The favored teeth in SEM have been the molars, both maxillary (upper)
or mandibular (lower). The location on the tooth does not seem to matter as long as it is a
facet that exhibits microwear. Impressions are then made of the molar using polysiloxane
vinyl, which is a compound used to make impressions in human dentistry. Casts are made
from the molds using an epoxy polymer. Specimens are examined under a standard light microscope to ensure that they are suitable for SEM. If the specimens are usable they are sputter-coated with silver to a thickness of five nanometers in order to be viewed under
the scanning-electron microscope. They are then placed under the scanning electron
microscope. Micrographs are taken at 500X and scanned into a computer at 200 dots-per-
inch. The features of the microwear are examined using the software program
MICROWEAR 4.0. The percentage incidence of pitting (pits are defined as microwear
scars with a length to width ratio of less than or equal to 4:1), scratch breadth, pit breadth
and pit length are all recorded. Then bivariate statistics, analysis of variance, and Mann-
Whitney U tests are employed to arrive at the results of the study.
There are a number of problems with using SEM to examine dental microwear.
Perhaps the most limiting factor is the expense of sample preparation and of the scanning
electron microscope itself (Godfrey et al., 2004; Semprebon et al., 2004). For example,
El-Zaatari (2005) examined 50 total specimens from eight species. Of those eight species,
two species were examined using only two specimens. Furthermore, large samples would
be challenging due to the time-intensive process of quantitatively measuring the width 23
and breadth of the microwear features (Godfrey et al., 2004). Therefore, any results drawn from these data tend to be based on small sample sizes. Gordon (1988) details a number of problems with the SEM technique in addition to the ones listed by Godfrey et al. (2004). These include the loss of resolution from the scanning electron microscope to the micrograph, the further loss of resolution to scan the micrograph into a computer, differences in magnification levels between studies, and limited visibility depending on the angle of the tooth under the microscope.
A newer method uses a scanning confocal microscopy (SCM) to generate three- dimensional images of the tooth surface. Scale-sensitive fractal analysis is then employed to characterize the microwear (Scott et al., 2005). Similar to SEM, a high quality cast is used. The cast is then placed into a white-light scanning confocal image profiler and recorded at 100X. The employment of graphical computer programs to analyze the results reduces inter-observer error, which is high in SEM. This also increases the sample sizes that may be examined by reducing the time needed to measure the microwear features. However, the SCM method is still reliant on the use of often prohibitively expensive equipment and software.
The newly developed low-magnification stereomicroscopy (LMS) method
(Godfrey et al., 2004; Semprebon et al., 2004) is in some regards more closely related to the pioneering study of Walker (1976) than to SEM or SCM. The general techniques summarized here are outlined by Semprebon and colleagues (2004). Molar teeth regardless of their origin (mandible or maxillae) are used for the analysis. The specimen casts are prepared just as in SEM and SCM. In LMS, however, the specimens are examined with a low-magnification stereomicroscope while an external fiber-optic light 24
source is manipulated to highlight the microwear features. The features are counted in a more categorical way than SEM features although the features that are recorded are
similar. Each specimen is sampled twice and averages of those samples are used for the
analyses. The purpose of taking two samples is to reduce sampling bias and limit the
effect of intra-observer error.
Semprebon (2004) notes that LMS is not meant to replace SEM. However, LMS
does overcome a number of the problems that are faced in SEM. In SEM, the most
significant limiting factor is cost. LMS is relatively inexpensive. The only equipment
needed is a standard microscope, an external light source and an ocular reticle (a 0.4 x 0.4 mm square placed in the eye piece of the microscope to define the sample area). This alone results in larger sample sizes. LMS is also more time efficient than SEM, since data are recorded categorically rather than being measured. Additionally, there is no lost resolution as data are recorded directly from the microscope without taking a micrograph and scanning it in to a computer. Stating a specific magnification in the initial paper on this method also eliminates the variation in magnification between studies. Finally, there
is no issue with the angle of the sample under the microscope limiting visibility. The
external light source can be manipulated in order to capture all the microwear features.
Microwear and Species Differentiation
Since the ground-breaking work of Semprebon and Godfrey (Godfrey et al., 2004;
Semprebon et al., 2004), other researchers have begun to apply this method to questions
that address niche and species differentiation (Godfrey et al., 2004; Proctor and Hudson,
2006; Williams et al., 2007). While the relationship between microwear and diet is fairly
concrete, the relationship between microwear and niche and species differentiation is less 25
intuitive. Since microwear is created by the food consumed by the individual, the comparative method can be used to infer diet in extinct forms. Once the dietary signals have been inferred some prediction can be made about the ecological niche that the animal occupied. Godfrey, et al. (2004) and Semprebon, et al. (2004) demonstrate how microwear can help place fossil primates into general dietary categories and then infer an ecological niche. The step to species differentiation is one degree further. Most species occupy a specific niche within their larger ecosystem. This is what allows many similar species to live sympatrically (Harcourt and Nash, 1986; Milton, 1981; Porter, 2001; Tutin and Fernandez, 2005). If differences between dental microwear in similar environments are present, perhaps this can help elucidate species differentiation among closely related forms. Additionally, if the phylogenetic species concept (Groves, 2004) is adhered to, microwear can serve as a proxy for the fixed character state that is needed to differentiate these species.
It should be noted that microwear alone cannot resolve the issue of species differentiation in these forms. However, this study combined with future studies may help to more clearly define the complex relationships of the species within these genera.
Microwear can help in proposing niche or species relationships that may serve as hypotheses for researchers investigating other traits.
Materials
A total of 188 individuals of 10 species of papionins, including three extant species of Papio, three extinct species of Papio, three extinct species of Parapapio and four individuals of an indeterminate Parapapio species were used in this study. Evidence from SEM studies that show some differences between adult and deciduous wear patterns 26
(Gordon, 2005; Perez-Perez et al., 2005). However, these findings are considered preliminary. Only adult specimens were used as there has been no published research involving the differences between the adult and deciduous teeth of specimens using LMS.
This will also serve to eliminate the possible confounding effects of ontogenetic changes related to diet (Godfrey et al., 2004). In order to maximize the sample size both upper and lower second molars were used. When possible, the paracone, or mesialmost buccal
(front-cheekside) cusp was used. However, in some instances the paracone was not available and other locations on the second molar were used. In other studies, no significant differences were found based on molar location (Godfrey et al., 2004;
Semprebon et al., 2004). See Appendix for a complete table of the specimens used.
Some species were combined in order to maximize the sample sizes for each species. For example, in the living baboons there are hybrid zones between Papio anubis and Papio hamadryas (Nystrom et al., 2004; Phillips-Conroy et al., 1991) as well as between Papio anubis and Papio cynocephalus (Samuels and Altmann, 1986). Some authors consider these baboons members of the same species with differences only at the subspecies level (Newman et al., 2003). Therefore, for this study P. anubis, P. hamadryas, and P. cynocephalus have been combined into the group called P. anubis.
The two other types of living baboons, P. ursinus and P. kindae were left as separate groups due to their evolutionary and geographic distance from the other baboons
(Newman et al., 2003). In the extinct baboon forms, some species designations (from the museums in which they are curated) were changed to match the current understanding of papionin phylogeny. P. wellsi has been eliminated in the literature and has been merged into P. izodi (Jablonski, 1994; Jablonski, 2002). Parapapio antiquus has also been 27
eliminated from the literature and reassigned to either Pp. broomi or Pp. whitei
(Jablonski, 2002). However, two specimens of Pp. antiquus were unable to be identified as an accepted species and have been placed into the category Pp. species indeterminate
(Pp. (sp.)). See table 1 for the individuals that were reassigned.
Table 1 – Reassigned Specimens
Specimen Was Is Justification MCZ 23082 P. cynocephalus P. anubis Hybrid zones MCZ 44276 P. cynocephalus P. anubis Hybrid zones MCZ 169 P. hamadryas P. anubis Hybrid zones MCZ 5008 P. hamadryas P. anubis Hybrid zones SAM 11728 P. wellsi P. izodi Condensed in literature SAM 11730 P. wellsi P. izodi Condensed in literature SAM 5356 P. wellsi P. izodi Condensed in literature TP 11 P. wellsi P. izodi Condensed in literature TP 9 Pp. antiquus Pp. whitei Not a real species T 17 Pp. antiquus Pp. broomi Not a real species TP 13 Pp. antiquus Pp. (sp) Not a real species TP 8 Pp. antiquus Pp. (sp) Not a real species
Method
The specimens were collected during several Georgia State University research
trips in 2005 to South Africa, Belgium, Massachusetts and the Netherlands headed by Dr.
Frank Williams. During this trip impressions were taken of the occlusal surface of each
specimen using polysiloxane vinyl. Once the materials were curated at Georgia State
University, casts were made using epoxy resin and hardener that had been run through a
centrifuge to eliminate air bubbles before casting. After allowing time to dry, the casts
were examined for microwear features under a standard low-magnification
stereomicroscope at 35X magnification. An external oblique (fiber-optic) light source
was manipulated to make the microwear features more visible. While under the
microscope, features that were within a 0.4 X 0.4 mm ocular reticle (a square that is
visible through the eyepiece) were counted following the procedures outlined in 28
Semprebon et al. (2004). The ocular reticle was positioned over a portion of the paracone
of the second molar (if available) that contained readable microwear. For each specimen
two samples were taken and then averaged together for use in the analyses.
The microwear features were classified as either pits or scratches. There is no
quantitative measurement for a pit, rather they are defined as features that are
approximately circular and have similar widths and lengths. Pits are broken into four
categories. Small pits are those that are only visible from the light reflected by them as
the oblique illumination is altered. Medium pits are those that are larger than a small pit
yet take up less than 1/4th of the ocular reticle. Large pits are those that take up at least
1/4th of the ocular reticle. Puncture pits are those that are very deep and craterlike and
have regular edges. They appear dark due to their depth. Scratches are also divided into
groups. Fine scratches are those that are narrow and finely etched into the surface of the
enamel. They are often only visible by manipulation of the light source. Coarse scratches are wider and deeper than fine scratches. Hypercoarse scratches are very deep, wide, and
trench-like. They appear dark regardless of the placement of the light source.
Statistical Analyses
After the data were collected statistical methods were employed to 1) determine if
the species designations that are assigned to specimens within the genera are statistically
real groups and to examine the taxonomic assignments using a new method 2) determine
what traits of the microwear can be used to differentiate species (if any), 3) determine if
there are redundant species labels, which may elucidate some of the temporal and scaling
issues in the papionins 4) determine if Papio and Parapapio can be distinguished using
dental microwear to examine possible ancestry between the genera and 5) to see if any 29
site or temporal differences exist, which may impact species designations or add information to the turnover pulse theory.
The data are first examined using a bivariate comparison of total pits versus total scratches to explore broad trophic patterns in the data. Determining if the species are statistically real groups is best facilitated by a discriminant function analysis (DFA).
Next, to understand which traits of the microwear differentiate species, an analysis of variance (ANOVA) with Tukey’s post hoc tests for Honestly Significant Differences
(HSD) was used. A principal components analysis (PCA) was utilized to see what groupings emerge from individuals’ factor scores. The PCA also identified variables that distinguish individuals. Determining if there are redundant species labels is largely dependent on the interpretation of the results of the analyses listed above, but also includes an examination of the descriptive statistics for each species to determine the amount of variation present in the sample. All of the above procedures were utilized again, but at the genera level to determine if Papio and Parapapio could be distinguished.
Finally, the same procedures were utilized based on site and then on time period. The use of these methods largely followed that of Godfrey et al. (2004). Each of these methods is discussed below.
Bivariate Analysis
Bivariate analyses were utilized in order to examine possible differences at broader levels. For example, total pits and total scratches were plotted in order to explore if species or even genera can be differentiated without breaking the pits and scratches into their components. These graphs include ellipses that represent a 95% confidence interval.
30
Analysis of Variance
Godfrey et al. (2004) uses an analysis of variance (ANOVA) with Tukey’s post
hoc test for HSD. The ANOVA reveals which microwear traits (small pits, coarse
scratches, etc.) are significantly different between all of the species. However, this level
of detail is not fine enough to determine among which species the differences lie. For that
reason a Tukey’s post hoc test for HSD is needed to examine all of the pairwise
comparisons. Tukey’s post hoc test for HSD was used rather than t-tests because for large
amounts of data (i.e. 10 species or 55 pairwise comparisons) the likelihood of finding
significant results by chance would be greater than the standard acceptable level of 0.05.
Tukey’s post hoc test for HSD takes into account this increasing likelihood and is thus a more conservative test for large sets of pairwise comparisons (Hill and Lewicki, 2006).
This analysis helps identify which microwear traits are useful for distinguishing groups.
Principal Components Analysis
A principal components analysis (PCA) is used to examine the
variance/covariance matrix to identify those traits which tend to polarize individuals (Hill
and Lewicki, 2006). The PCA reduces the data to fewer dimensions, which reveals how
the variation within and across individuals and traits is partitioned. The PCA does not
consider the species labels, which have been assigned, but rather groups specimens based
solely on the variance/covariance of multiple traits. By extracting principal components
from the data, new variables are formed. The purpose of this is to “maximize the variance
(variability) of the ‘new’ variable (factor), while minimizing the variance around the new
variable” (Hill and Lewicki, 2006). This allows for the major components of variability
to be revealed and graphed against each other. This shows which components polarize 31
individuals and sheds light into group clusters. The PCA graphs include ellipses that represent 95% confidence intervals.
Discriminant Function Analysis
Following Godfrey et al. (2004), the final statistical analysis employed is a discriminant function analysis (DFA). The DFA assumes that there are “real” groups within the data and then examines which variables are the most predictive of membership in one of the “real” groups. In this way, the individuals were examined to determine if they fell into the group to which they were assigned. If the DFA did not predict group membership, this suggests that the groupings may not be accurate.
32
Chapter Four: Results
Results by Species
Bivariate Comparision
The initial comparison of the groups was done by plotting total pits against total scratches, which is standard in the literature. As seen in Figure 1, the relationship among these species is tightly linked. Little can be gathered from this graph beyond a few rough details. P. angusticeps appears to have the least variation and is differentiated by having fewer microwear features than other species. P. robinsoni, has slightly more variation, but also generally has fewer microwear features. However, the variation of P. angusticeps and P. robinsoni overlap significantly. In fact, all of the species overlap
Figure 1 – Bivariate Graph of Total Pits and Scratches by Species 33
to some extent. Two of the extant species, P. anubis and P. ursinus have the largest amounts of variation. That should be expected due to their relatively large geographic ranges and the larger sample of extant specimens. However, the third extant species, P.
kindae has a smaller amount of variation and a smaller geographic range than the other
living forms. This suggests that P. kindae either has a more specialized diet than P. ursinus and P. anubis and thus lives in a smaller geographic area or that P. kindae is restricted to a smaller geographic area that happens to have a slightly different ecosystem resulting in different microwear signals. This supports separating P. kindae from other
Papio taxa because living species that occupy different ecosystems can be classified as
different species.
There are also differences between the living forms and the fossil forms. Living
forms such as P. ursinus and P. anubis exhibit more scratches and fewer pits than the
extinct forms of both Papio and Parapapio. These differences are explored in the genera
and temporal analyses.
ANOVA with Tukey’s HSD
Table 2 shows the sample size, mean and standard deviation by species for each
of the microwear traits that were examined. The ANOVA (Table 3) between species
revealed significant (p < 0.05) differences for the following microwear features: medium
pits, fine scratches, coarse scratches, hypercoarse scratches and total scratches. The
significant species differences that were revealed in the Tukey’s post hoc test for
Honestly Significant Differences are shown in Table 4. There were no significant
differences found among small pits, large pits, puncture pits and total pits. As such, they
will not be included in Table 4 nor any further analyses. 34
Table 2 – Mean and Standard Deviation of Microwear Features by Species
Species Sm. Pits Med. Pits Lg. Pits Punct. Pits Tot. Pits Fine Scratch Coarse Scratch H.coarse Scratch Tot. Scratch P. angusticeps Mean 3.219 0.875 0.063 0 4.156 1.313 0.781 0.188 2.281 N=16 Std. Dev. 2.5428 0.7638 0.1708 0 2.7732 0.9979 0.5154 0.3096 0.9656 P. anubis Mean 3.75 1.389 0 0 5.139 2.806 1.694 0.639 5.139 N=18 Std. Dev. 2.3964 1.2897 0 0 2.5426 1.8242 1.1264 0.6818 2.412 P. izodi Mean 2.4 1 0 0 3.4 2.8 0.9 0 3.7 N=5 Std. Dev. 0.8216 0.7071 0 0 0.8216 2.1389 0.7416 0 1.7176 P. kindae Mean 2.659 1.591 0 0.045 4.295 3.068 1.591 0.295 4.955 N=22 Std. Dev. 2.5232 1.4196 0 0.1471 3.1155 2.1564 1.1916 0.427 2.4684 P. robinsoni Mean 3.976 0.595 0.048 0.024 4.643 0.929 1.238 0.286 2.452 N=21 Std. Dev. 2.5859 0.7845 0.2182 0.1091 3.0665 0.9258 0.718 0.4351 1.0595 P. ursinus Mean 3.15 1.183 0 0 4.333 3.817 1.367 0.333 5.517 N=30 Std. Dev. 1.609 1.0379 0 0 1.877 2.4792 1.2861 0.5622 3.1058 Pp. (sp) Mean 1.625 0.875 0 0 2.5 2.625 0.75 0.375 3.75 N=4 Std. Dev. 1.493 0.4787 0 0 1.472 1.7017 0.6455 0.4787 1.1902 Pp. broomi Mean 3.48 1.58 0 0.04 5.1 2.02 2.14 0.22 4.38 N=25 Std. Dev. 2.5596 1.3124 0 0.1384 2.8062 1.6361 1.3733 0.4805 2.098 Pp. jonesi Mean 2.818 1.364 0.023 0 4.205 2.591 1.818 0.114 4.523 N=22 Std. Dev. 1.8228 1.5367 0.1066 0 2.8605 1.5708 1.3848 0.2642 1.8092 Pp. whitei Mean 2.44 2.5 0 0 4.94 2.02 2.04 0.2 4.26 N=25 Std. Dev. 1.46 2.586 0 0 3.1336 1.2787 1.4356 0.3227 1.6401 Total Mean 3.106 1.396 0.013 0.013 4.529 2.423 1.58 0.274 4.277 N=188 Std. Dev. 2.1698 1.5168 0.0958 0.0807 2.7107 1.9252 1.2363 0.4633 2.319
Table 3 – ANOVA Results for Species
Sum of Squares df Mean Square F Sig. Sm. Pits Between Groups 55.696 9 6.188 1.336 0.221 Within Groups 824.676 178 4.633 Total 880.372 187 Med. Pits Between Groups 53.212 9 5.912 2.791 0.004 Within Groups 377.016 178 2.118 Total 430.227 187 Lg. Pits Between Groups 0.088 9 0.01 1.072 0.386 Within Groups 1.629 178 0.009 Total 1.717 187 Punct. Pits Between Groups 0.064 9 0.007 1.1 0.365 Within Groups 1.153 178 0.006 Total 1.217 187 Tot. Pits Between Groups 49.07 9 5.452 0.732 0.679 Within Groups 1325.019 178 7.444 Total 1374.089 187 Fine Scratch Between Groups 146.307 9 16.256 5.292 0 Within Groups 546.825 178 3.072 Total 693.132 187 Coarse Scratch Between Groups 33.712 9 3.746 2.645 0.007 Within Groups 252.091 178 1.416 Total 285.803 187 H.coarse Scratch Between Groups 3.827 9 0.425 2.084 0.033 Within Groups 36.316 178 0.204 Total 40.142 187 Tot. Scratch Between Groups 207.593 9 23.066 5.145 0 Within Groups 798.024 178 4.483 Total 1005.617 187
35
Table 4 – Significant Results from Tukey’s HSD by Species
95% Confidence Interval Dependent Variable Species Species Mean Difference (I-J) Std. Error Sig. Lower BoundUpper Bound Medium Pits P. angusticeps Pp. whitei -1.6250(*) 0.4659 0.021 -3.118 -0.132 P. robinsoni Pp. whitei -1.9048(*) 0.4308 0.001 -3.285 -0.524 P. ursinus Pp. whitei -1.3167(*) 0.3941 0.033 -2.580 -0.054 Fine Scratches P. angusticeps P. ursinus -2.5042(*) 0.5426 0.000 -4.243 -0.766 P. anubis P. robinsoni 1.8770(*) 0.5630 0.034 0.073 3.681 P. robinsoni P. kindae -2.1396(*) 0.5347 0.004 -3.853 -0.426 P. robinsoni P. ursinus -2.8881(*) 0.4987 0.000 -4.486 -1.290 Pp. broomi Pp. whitei 1.7967(*) 0.4746 0.008 0.276 3.318 Pp. broomi P. ursinus -1.7967(*) 0.4746 0.008 -3.318 -0.276 Pp. whitei P. ursinus -1.7967(*) 0.4746 0.008 -3.318 -0.276 Coarse Scratches P. angusticeps Pp. broomi -1.3588(*) 0.3810 0.016 -2.580 -0.138 P. angusticeps Pp. whitei -1.2588(*) 0.3810 0.037 -2.480 -0.038 H.coarse Scratches P. anubis Pp. jonesi .5253(*) 0.1436 0.012 0.065 0.985 Total Scratches P. angusticeps P. anubis -2.8576(*) 0.7275 0.005 -5.189 -0.526 P. angusticeps P. kindae -2.6733(*) 0.6957 0.006 -4.903 -0.444 P. angusticeps P. ursinus -3.2354(*) 0.6555 0.000 -5.336 -1.135 P. angusticeps Pp. jonesi -2.2415(*) 0.6957 0.048 -4.471 -0.012 P. anubis P. robinsoni 2.6865(*) 0.6801 0.004 0.507 4.866 P. kindae P. robinsoni 2.5022(*) 0.6460 0.006 0.432 4.572 P. robinsoni P. ursinus -3.0643(*) 0.6024 0.000 -4.995 -1.134 P. robinsoni Pp. jonesi -2.0703(*) 0.6460 0.050 -4.140 0.000 *. The mean difference is significant at the .05 level.
Principal Components Analysis
The data are made complex by a large number of zeros. This may initially appear
as missing data. However, since there were zero microwear features observed this is in
fact data (Allison, 2001). Fortunately, most of the zeros found in the data set were in the
categories of large and puncture pits, which were not significant and were eliminated
from the analyses. The other category that has a large amount of zeros is hypercoarse
scratches. While this results in a slight positive skew of the variance/covariance matrix,
this category does discriminate among species, so it will remain in the data set despite the
presence of the zeros. 36
The PCA resulted in five principal components, two of which had Eigenvalues over one. The components with Eigenvalues less than one will not be considered. The first principal component axis polarizes total and fine scratches positively and medium pits negatively (See Table 5 for component loadings). This axis explains 42.24% of the variation. The second principal component axis polarizes hypercoarse scratches positively and coarse scratches and medium pits negatively. This axis explains 21.80% of the variance. See Figure 2.
Table 5 – PCA Component Loadings by Species
Component 12 Total Scratches 0.977 0.055 Fine Scratches 0.825 0.102 Coarse Scratches 0.579 -0.382 Hypercoarse Scratches -0.08 0.871 Medium Pits -0.369 -0.414 Extraction Method: Principal Component Analysis. a. 2 components extracted.
37
Figure 2 – Graph of PCA Axes 1 and 2 by Species
This analysis reveals that P. angusticeps is again the species with the least
variation and P. robinsoni has the second least variation. However, P. robinsoni is now
differentiated from P. angusticeps by being polarized from having more hypercoarse scratches, while P. angusticeps is polarized by fine and total scratches. However, these two species still fall within the variation that is present in all the other species. P. ursinus
and P. anubis again have the most variation.
Discriminant Function Analysis
The DFA resulted in four canonical functions, which captured 100% of the variation. The first discriminant function explains 56.0% of the variance in the data. The first three functions together explain 97.0% of the data. 38
The post hoc classification success for the sample of 188 individuals was 27.1%
based on the discriminant functions. In other words, the DFA correctly grouped the
species 17.1 percentage points above chance. See Table 6 for a summary of how each
species was classified.
Table 6 – DFA Classification Results by Species
Predicted Group Membership (a) P. P. P. P. P. Pp. Pp. Pp. Pp. Species angusticeps anubis P. izodi kindae robinsoni ursinus (sp) broomi jonesi whitei Total Original Count P. angusticeps 7 020 3 0400016 P. anubis 1 6 21 1 3011218 P. izodi 1010 12 00005 P. kindae 0 441131224 22 P. robinsoni 4320 9 01 1 1 0 21 P. ursinus 4531 310 013030 Pp. (sp) 002 01010004 Pp. broomi 1441 020 7 1525 Pp. jonesi 1150 121 6 2322 Pp. whitei 0311 112547 25 % P. angusticeps 43.8 0.0 12.5 0.0 18.8 0.0 25.0 0.0 0.0 0.0 100.0 P. anubis 5.6 33.3 11.1 5.6 5.6 16.7 0.0 5.6 5.6 11.1 100.0 P. izodi 20.0 0.0 20.0 0.0 20.0 40.0 0.0 0.0 0.0 0.0 100.0 P. kindae 0.0 18.2 18.2 4.5 4.5 13.6 4.5 9.1 9.1 18.2 100.0 P. robinsoni 19.0 14.3 9.5 0.0 42.9 0.0 4.8 4.8 4.8 0.0 100.0 P. ursinus 13.3 16.7 10.0 3.3 10.0 33.3 0.0 3.3 10.0 0.0 100.0 Pp. (sp) 0.0 0.0 50.0 0.0 25.0 0.0 25.0 0.0 0.0 0.0 100.0 Pp. broomi 4.0 16.0 16.0 4.0 0.0 8.0 0.0 28.0 4.0 20.0 100.0 Pp. jonesi 4.5 4.5 22.7 0.0 4.5 9.1 4.5 27.3 9.1 13.6 100.0 Pp. whitei 0.0 12.0 4.0 4.0 4.0 4.0 8.0 20.0 16.0 28.0 100.0 a. 27.1% of original grouped cases correctly classified.
Results by Genera
For the analyses by genera the total sample remains the same (n=188). There are
112 specimens of Papio and 76 specimens of Parapapio.
Bivariate Comparison
Total pits and total scratches were graphed against each other by genera. See
Figure 3. This graph reveals a significant amount of overlap between the two genera.
However, Papio exhibits more scratches and fewer pits than Parapapio. Godfrey et al.
(2004) found that few scratches and some pits indicate a diet that consists of leaves and 39
some fruit while more scratches and fewer pits indicate more grasses and less fruit in the diet. This suggests that Parapapio may have focused on a more arboreal diet than Papio.
Figure 3 – Bivariate Graph of Total Pits and Scratches by Genera
ANOVA
Table 7 shows the results for the ANOVA run at the genus level (Papio and
Parapapio). Significant differences were only found between the genera on the microwear traits of medium pits and coarse scratches. However, hypercoarse scratches approach significance (p = .052) and will be considered in the analyses. The microwear features that were not significant will not be considered further. 40
Table 7 – ANOVA Results for Genera
Sum of Squares df Mean Square F Sig. Sm. Pits Between Groups 9.303 1 9.303 1.986 0.16 Within Groups 871.069 186 4.683 Total 880.372 187 Med. Pits Between Groups 21.015 1 21.015 9.552 0.002 Within Groups 409.212 186 2.2 Total 430.227 187 Lg. Pits Between Groups 0.005 1 0.005 0.596 0.441 Within Groups 1.711 186 0.009 Total 1.717 187 Punct. Pits Between Groups 0 1 0 0 0.996 Within Groups 1.217 186 0.007 Total 1.217 187 Tot. Pits Between Groups 2.133 1 2.133 0.289 0.591 Within Groups 1371.956 186 7.376 Total 1374.089 187 Fine Scratch Between Groups 5.479 1 5.479 1.482 0.225 Within Groups 687.653 186 3.697 Total 693.132 187 Coarse Scratch Between Groups 18.676 1 18.676 13.004 0 Within Groups 267.127 186 1.436 Total 285.803 187 H.coarse Scratch Between Groups 0.811 1 0.811 3.834 0.052 Within Groups 39.332 186 0.211 Total 40.142 187 Tot. Scratch Between Groups 1.168 1 1.168 0.216 0.642 Within Groups 1004.449 186 5.4 Total 1005.617 187
Principal Components Analysis
The PCA resulted in three principal components, two of which had Eigenvalues over one. See Table 8 for the component loadings. The first PCA axis polarizes medium pits and hypercoarse scratches positively and coarse scratches negatively. The second
PCA axis polarizes medium pits positively and hypercoarse scratches negatively. See
Figure 4. Axis 1 explains 38.89% of the variance. PCA axes 1 and 2 together explain
74.64% of the variance.
41
Table 8 – PCA Component Loadings by Genera
Component (a) 12 Coarse Scratch -0.828 -2.90E-02 Med. Pits 0.454 0.76 H.coarse Scratch 0.525 -0.702 Extraction Method: PCA a. 2 components extracted.
Figure 4 – Graph of PCA Axes 1 and 2 by Genera
In this analysis Papio and Parapapio again have a significant amount of overlap.
However, there are slight differences. Parapapio has a broader range on PCA axis 1, which means there is more variation in the microwear features of hypercoarse scratches and medium pits positively and coarse scratches negatively. Papio is polarized by having more medium pits on PCA axis 2. 42
Discriminant Function Analysis
The DFA resulted in one canonical function, which captured 100% of the
variation. The post hoc classification success for the sample of 188 individuals was
66.5% based on the discriminant functions. The classification was 16.5 percentage points above chance. See Table 9 for classification results by genera.
Table 9 – DFA Classification Results by Species
Membership
Genera Papio Parapapio Total Original Count Papio 82 31 113 Parapapio 32 43 75 % Papio 72.6 27.4 100.0 Parapapio 42.7 57.3 100.0 a. 66.5% of original grouped cases correctly classified.
Results by Site
The site locations for all of the extinct specimens are known. However, it is less
clear exactly where the living specimens were collected. Therefore, the living species
have been grouped into regional sites. In this manner, Papio anubis is from East-Central
Africa, Papio kindae is from Central Africa and Papio ursinus is from Southern Africa.
While these regional site designations are not as specific as the site locations for the
extinct specimens, they will still serve to differentiate the groups. See Table 10 for the
sample size by site.
43
Table 10 – Sample Size by Site
Valid Frequency Percent Bolt's Farm 2 1.1 Central Africa 22 11.7 Cooper's Cave 12 6.4 East-Central Africa 18 9.6 Kromdraai 7 3.7 Makapansgat 8 4.3 Southern Africa 30 16.0 Sterkfontein 49 26.1 Swartkrans 29 15.4 Taung 11 5.9 Total 188 100.0
Bivariate Comparison
The initial comparison was the bivariate graph of total pits and total scratches by
site. See Figure 5. At this level of analysis Cooper’s Cave, Taung, Bolt’s Farm and
Kromdraai have the tightest groupings. However, Bolt’s Farm has the smallest sample
size (n = 2) in the analysis. With only two data points a tight cluster does not seem
reliable. Cooper’s Cave (n = 12), Taung (n = 11) and Kromdraai (n = 7) are more robust
in their clustering. There is once again, significant overlap in these groupings. The sites
of Central Africa, East-Central Africa, and Southern Africa have the most variation.
Since these are regional sites more variation was expected than what was found in the specific cave sites. When analyzing the data at this level, the extant regional sites do not have the largest sample size as they did in the species and genera level analyses.
Sterkfontein has the largest sample (n = 49) and has less variation than the living species.
This suggests that there are more dietary similarities between the species found at
Sterkfontein than among the living baboon groups.
44
Figure 5 – Bivariate Graph of Total Pits and Scratches by Site
ANOVA with Tukey’s HSD
The ANOVA (Table 11) between sites revealed significant differences (p < 0.05) among medium pits, fine scratches, coarse scratches, hypercoarse scratches and total scratches. These are the same microwear features that were found to be significant in the species level analysis. The features that are not significant will not be considered further.
The site differences that were revealed in the Tukey’s post hoc test for Honestly
Significant Differences are shown in Table 12. 45
Table 11 – ANOVA Results for Site
Sum of Squares df Mean Square F Sig. Sm. Pits Between Groups 47.725 9 5.303 1.134 0.341 Within Groups 832.648 178 4.678 Total 880.372 187 Med. Pits Between Groups 62.002 9 6.889 3.33 0.001 Within Groups 368.225 178 2.069 Total 430.227 187 Lg. Pits Between Groups 0.09 9 0.01 1.09 0.372 Within Groups 1.627 178 0.009 Total 1.717 187 Punct. Pits Between Groups 0.041 9 0.005 0.694 0.714 Within Groups 1.176 178 0.007 Total 1.217 187 Tot. Pits Between Groups 87.055 9 9.673 1.338 0.22 Within Groups 1287.034 178 7.231 Total 1374.089 187 Fine Scratch Between Groups 127.182 9 14.131 4.445 0 Within Groups 565.95 178 3.179 Total 693.132 187 Coarse Scratch Between Groups 30.502 9 3.389 2.363 0.015 Within Groups 255.301 178 1.434 Total 285.803 187 H.coarse Scratch Between Groups 4.041 9 0.449 2.214 0.023 Within Groups 36.101 178 0.203 Total 40.142 187 Tot. Scratch Between Groups 178.3 9 19.811 4.262 0 Within Groups 827.317 178 4.648 Total 1005.617 187
Table 12 – Significant Results from Tukey’s HSD by Site
Interval Lower Upper Dependent Variable (I) Site (J) Site Mean Difference (I-J) Std. Error Sig. Bound Bound Med. Pits Cooper's Cave Makapansgat -2.2917(*) 0.6565 0.021 -4.395 -0.188 Makapansgat South Africa 1.9417(*) 0.5723 0.029 0.108 3.776 Swartkrans 2.5388(*) 0.5744 0.001 0.698 4.379 Sterkfontein Swartkrans 1.2607(*) 0.3370 0.009 0.181 2.340 Fine Scratch Cooper's Cave South Africa -2.4833(*) 0.6090 0.003 -4.435 -0.532 South Africa Sterkfontein 1.7248(*) 0.4134 0.002 0.400 3.049 Swartkrans 2.3339(*) 0.4643 0.000 0.846 3.822 Coarse Scratch Cooper's Cave Sterkfontein -1.4456(*) 0.3857 0.009 -2.682 -0.210 East-Central H.coarse Scratch Sterkfontein Africa -.4144(*) 0.1241 0.034 -0.812 -0.017 Tot. Scratch Central Africa Cooper's Cave 2.7879(*) 0.7737 0.015 0.309 5.267 East-Central Cooper's Cave Africa -2.9722(*) 0.8035 0.011 -5.547 -0.398 South Africa -3.3500(*) 0.7364 0.000 -5.710 -0.990 Sterkfontein -2.2619(*) 0.6944 0.043 -4.487 -0.037 South Africa Swartkrans 2.3615(*) 0.5614 0.002 0.563 4.160 *. The mean difference is significant at the .05 level. 46
Principal Components Analysis
A separate PCA is not needed in order to examine the results by site because the
site level analysis uses the same significant features found in the initial PCA run at the
species level. However, those results can be graphed by site (Figure 6).
Bolt’s Farm, Cooper’s Cave and Kromdraai are the most tightly clustered. This is
similar to what was found in the bivariate comparison. However, these tighter clusters are
found in the range of all the other sites. East-Central Africa and South Africa have the
most variation. Makapansgat is slightly differentiated from the other groupings by being
polarized negatively on both PCA axes 1 and 2. That is, Makapansgat specimens tend to have more medium pits and coarse scratches.
Figure 6 – Graph of PCA Axes 1 and 2 by Site
47
Discriminant Function Analysis
The DFA resulted in four canonical functions, which captured 100% of the variation. The post hoc classification success for the sample of 188 individuals was
30.9% based on the discriminant functions. The classification results are 20.9 percentage points above chance. See Table 13 for classification results by site.
Table 13 – DFA Classification Results by Site
Predicted Group Membership (a) Site Bolt's Farm C. Africa Cooper's Cave E.C. Africa Kromdraai Makapansgat S. Africa Sterkfontein Swartkrans Taung Total Original Count Bolt's Farm 2 0 000 000002 C. Africa 1 2 0 3 1 3 5 32222 Cooper's Cave 1 0 8 01 0001112 E.C. Africa 3 1 1 4 11330118 Kromdraai 1 0 1 0 3 00 0 117 Makapansgat 0 1 0 0 0 3 0 3 108 S. Africa 2 2 4 4 0 1 10 13330 Sterkfontein 2 0 1 6 6 9 6 13 2449 Swartkrans 4 0 6 1 2 0 0 3 10 329 Taung20 101 11113 11 % Bolt's Farm 100 0 000 00000100 C. Africa 4.5 9.1 0 13.6 4.5 13.6 22.7 13.6 9.1 9.1 100 Cooper's Cave 8.3 0 66.7 0 8.3 0 0 0 8.3 8.3 100 E.C. Africa 16.7 5.6 5.6 22.2 5.6 5.6 16.7 16.7 0 5.6 100 Kromdraai 14.3 0 14.3 0 42.9 0 0 0 14.3 14.3 100 Makapansgat 0 12.5 0 0 0 37.5 0 37.5 12.5 0 100 S. Africa 6.7 6.7 13.3 13.3 0 3.3 33.3 3.3 10 10 100 Sterkfontein 4.1 0 2 12.2 12.2 18.4 12.2 26.5 4.1 8.2 100 Swartkrans 13.8 0 20.7 3.4 6.9 0 0 10.3 34.5 10.3 100 Taung 18.2 0 9.1 0 9.1 9.1 9.1 9.1 9.1 27.3 100 a. 30.9% of original grouped cases correctly classified.
Results by Time Period
The dating of these sites is imprecise, so grouping species by absolute time is difficult. The best estimates for the dates of these sites come from Delson (1984) and
Williams et al. (2007). To simplify the complex temporal relationships a bivariate grouping of extinct and extant is used to represent relative time periods. There are 118 extinct specimens and 70 extant specimens.
48
Bivariate Comparison
The initial comparison was done by plotting total pits and total scratches by status
(extinct or extant). See Figure 7. The extinct specimens have fewer scratches than the extant specimens. This could support Vrba’s (1983, 1993, 1996) turnover pulse hypothesis by demonstrating that extinct species have less grit in their diet than extant species species. This suggests that the Plio-Pleistocene climate shift from a wetter, more wooded environment to a drier more savanna habitat had an impact on the diet of these species. Additionally, the dietary categories presented by Godfrey et al. (2004) support these data. Grass eaters have a high number of scratches and low numbers of pits, while leaf eaters have fewer scratches and slightly more pits. If these categories are accepted, extant species with more scratches could be classified as more grass-eating, which is indicative of their savanna habitat, while the extinct species with fewer scratches and more pits could be considered more leaf-eating, which would support them living in a more wooded environment.
49
Figure 7 – Bivariate Graph of Total Pits and Scratched by Time Period
ANOVA
The ANOVA (Table 14) between extinct and extant species revealed significant differences (p < 0.05) for the microwear features of fine scratches, hypercoarse scratches, and total scratches. The microwear features that are not significant will not be considered further.
50
Table 14 – ANOVA Results for Time Period
Sum of Squares df Mean Square F Sig. Sm. Pits Between Group 0.212 1 0.212 0.045 0.833 Within Groups 880.16 186 4.732 Total 880.372 187 Med. Pits Between Group 0.114 1 0.114 0.049 0.824 Within Groups 430.113 186 2.312 Total 430.227 187 Lg. Pits Between Group 0.02 1 0.02 2.162 0.143 Within Groups 1.697 186 0.009 Total 1.717 187 Punct. Pits Between Group 0 1 0 0.017 0.898 Within Groups 1.217 186 0.007 Total 1.217 187 Tot. Pits Between Group 0 1 0 0 0.998 Within Groups 1374.089 186 7.388 Total 1374.089 187 Fine Scratch Between Group 90.046 1 90.046 27.771 0 Within Groups 603.086 186 3.242 Total 693.132 187 Coarse Scratch Between Group 0.38 1 0.38 0.248 0.619 Within Groups 285.423 186 1.535 Total 285.803 187 H.coarse ScratcBetween Group 1.772 1 1.772 8.592 0 Within Groups 38.37 186 0.206 Total 40.142 187 Tot. Scratch Between Group 104.127 1 104.127 21.484 0 Within Groups 901.49 186 4.847 Total 1005.617 187
Principal Components Analysis
The PCA resulted in three principal components, two of which had Eigenvalues over one. The component loadings are shown in Table 15. PCA axis 1 polarizes fine and total scratches positively and hypercoarse scratches negatively. PCA axis 2 polarizes hypercoarse scratches positively and fine scratches negatively. See Figure 8. Axis 1 explains 61.40% of the variance. Axes 1 and 2 together explain 95.07% of the variance.
51
Table 15 – PCA Component Loadings by Time Period
Component (a) 12 Fine Scratch 0.961 -5.34E-02 Tot. Scratch 0.957 0.108 H.coarse Scratch -5.22E-02 0.998 Extraction Method: Principal Component a. 2 components extracted.
Figure 8 – Graph of PCA Axes 1 and 2 by Time Period
As in the bivariate graph, the extant species are polarized by fine and total scratches positively on PCA axis 1 and hypercoarse scratches positively on PCA axis 2.
In other words, the extinct species have fewer scratches than the extant species. Once again this supports the turnover-pulse hypothesis (Vrba 1983, 1993, 1996) and the dietary categories presented by Godfrey et al. (2004). 52
Discriminant Function Analysis
The DFA resulted in one canonical function, which explained 100% of the
variance. The post hoc classification success for the sample of 188 individuals was 66.0% based on the discriminant functions. Since only two time states, extinct and extant, were used, a random distribution of the specimens would have resulted in a 50% success rate.
The actual classification success is 16 percentage points above chance. See Table 16 for a summary of the classification results.
Table 16 – DFA Classification Results by Time Period
Predicted Group Membership Living or Dead Extinct Extant Total Original Count Extinct 81 37 118 Extant 27 43 70 % Extinct 68.6 31.4 100 Extant 38.6 61.4 100 a. 66.0% of original grouped cases correctly classified.
53
Chapter Five: Discussion and Conclusions
Discussion
This study has attempted to answer a number of questions regarding the taxonomic and temporal differences of the southern African papionins from the Plio-
Pleistocene to the present using dental microwear. A number of arguments can be made based on the results. The extinct forms of Papio have less variation than would be expected and may be representative of one species. Parapapio forms cannot be distinguished based on dental microwear and may represent one species with temporal variation. Makapansgat appears older than the other sites examined due to the relatively high frequency of pits, representing fruit, found in the specimens from that site. Finally, a turn-over pulse is evident when the extinct forms are compared to the extant forms. These results are discussed at length below.
Species
The bivariate analysis and the PCA resulted in graphs with large amounts of overlap in the data. All of the species fall within the same general range of pits and scratches with no species having a clearly different microwear signature from any other species. However, three species, P. angusticeps, P. robinsoni, and P. izodi, which are the extinct Papio forms, are more tightly clustered than the rest of the species. This may be problematic in their classification as separate species. Godfrey and Marks (1991) noted that extinct species should have no more variation than their extant relatives. The inverse may also be true. P. robinsoni, P. angusticeps, and P. izodi fall within the range of 54
variation of the extant species examined and have less variation than those extant species.
It may be possible that these species should be reexamined to see if, when combined,
these three species would form one species whose variation would mirror that found in extant species. The DFA somewhat confirms that the three extinct forms of Papio may be indicative of one group, as they are misclassified at least 18.8% of the time as each other
(Table 6). This is even more compelling taken in light of their respective locations. There is no duplication of extinct Papio from any one site in this study. In light of the dental microwear evidence, it may be possible that researchers have seen site differences in these forms and have attributed that incorrectly to species differences.
A similar issue arises when looking at the three Parapapio forms. These forms evidence significant overlap in their variation and the variation is essentially the same when examined both in a bivariate manner and with PCA. The variation in these forms is more similar to what is found in the extant species, but could encompass more variation.
This suggests they belong to a single species. However, this is complicated by the fact that these species often occur at the same sites. The past differences that have been observed may not be attributed to site differences. The literature acknowledges that with
Parapapio there are concerns about these species since they are essentially scaled versions of each other (Freedman, 1976) and may represent either chronological or ecogeographic differences rather than species differences. The DFA confirmed these results as the species Pp. jonesi (27.3%) and Pp. whitei (20.0%) are often identified as
Pp. broomi. The three species of Parapapio should be reexamined in light of this new evidence to determine if there are enough differences to warrant three species. 55
This result contradicts the findings of El-Zaatari et al. (2005) and supports the
findings of Williams et al. (2007). El-Zaatari et al. (2005) found site differences between the Parapapio specimens using SEM but did not address the range of variation that is acceptable within a species. However, the sample sizes used by El-Zaatari et al. (2005) are much smaller than those used here.
Williams et al. (2007) uses facial affinities to form a biochronology of Parapapio.
They argue that there are no significant differences in facial traits between Pp. broomi
and Pp. whitei, corroborating this study. Williams et al. (2007) finds a facial difference in
one specimen (STS 565) of Pp. jonesi, but argues that difference is likely due to temporal
variation.
Genera
The bivariate and PCA graphs of genera also reveal significant overlap of the
specimens. However, there are noticeable differences between the genera. Papio has
more scratches and fewer pits than Parapapio. According to the dietary categories of
Godfrey et al. (2004), this implies that Papio is more dependent on grasses while
Parapapio was somewhat more reliant on leaves and fruit. This confirms the results of
El-Zaatari et al. (2005) who also found fewer pits and more scratches in the living forms
than the extinct forms. It should be noted, however that the same specimens were not
used.
This result may support Vrba’s (1983, 1993, 1996) turnover pulse hypothesis. The
older forms (Parapapio) consume foods that are indicative of a more wooded habitat
while the younger forms (Papio) consume foods that are indicative of a more savanna-
like habitat. However, there are extinct forms of Papio included in this analysis that 56
confound the results. That is, because extinct forms of Papio, that lived before or during
the Plio-Pleistocene climate shift, had similar features to extant forms of Papio, that lived
after the climate shift, either climate change did not influence Papio as strongly as would
be suggested by the turnover pulse hypothesis or an even stronger result would be found
by examining explicit temporal differences.
Site
The bivariate comparison resulted in groups that significantly overlapped. The
tightest groupings were from the sites with the fewest samples. However, the site with the
most samples, Sterkfontein, had less variation than the regional sites of the extant species.
This may suggest an ecological microniche at Sterkfontein that results in less dietary
variation than would be expected or that specimens from Sterkfontein had a more focused
diet than the modern papionins.
The PCA revealved similar results that included significant overlap and the
greatest variation found in the regional sites of the extant forms. However, Makapansgat
is slightly differentiated by having more medium pits and coarse scratches than the other
sites. The only species observed here from Makapansgat are Pp. broomi and Pp. whitei.
This may support the climactic and dietary differences found between the older and more
recent forms by suggesting that this site with only Parapapio shows more of a
concentration on fruit than the other sites. This further suggests that Makapansgat is an
older site than the others since the microwear features from specimens at this site are
indicative of a more frugivorous diet. However, this is difficult to ascertain due to the
range of species that occur at other sites. 57
The DFA correctly classifies nine out of 10 sites (at least 26.5% and up to 100%, or 20.9 percentage points above chance, see Table 13) the majority of the time. This is the strongest result of all the DFA’s in the study. This indicates that site location must be taken into account in any further studies that examine these species. Because the DFA is most successful at grouping species by site, there must be microwear features that are site specific.
It is possible that the site differences actually show temporal variation. Just as
Makapansgat appears to be an older site based on the microwear dietary signals, other
Pliocene sites, such as Bolt’s Farm, Sterkfontein and Taung, may be differentiated from the younger Pleistocene sites of Kromdraai and Swartkrans (Williams et al., 2007).
Time Period
Perhaps the clearest results come from the analysis by gross time period, or whether the species is extinct or extant. Both the bivariate analysis and the PCA show clear differences between the extinct and extant forms. This is similar to what was found in the genus level analysis that older forms (Parapapio) exhibit microwear features that are indicative of a more frugivorous diet than the younger forms (Papio). However, using an extinct/extant comparison eliminates the extinct Papio bias found in the genus level analysis. The extinct forms have fewer scratches and slightly more pits than the extant forms. The dietary signal (Godfrey et al., 2004) shown by the extinct forms shows a focus on leaves and some fruit while the signal shown by the extant forms shows more of a reliance on grasses and the accompanying grit in their diet. This clearly shows an ecological shift from a more wooded environment to a more savanna environment and 58
becomes clear support for Vrba’s (1983, 1993, 1996) turnover-pulse hypothesis as well as
confirming continued climate deterioration later in the Pleistocene to the present day.
Conclusions
As noted by Carter (2006), a limitation of LMS dental microwear is that it cannot
explain individual differences in diet. Rather, it is more appropriate to examine
populations with large enough sample sizes. Despite this limitation, LMS still has
significant advantages over SEM and SCM. While LMS may not be as precise as other
methods, it can increase sample sizes and supplement the results of other methods.
However, extreme precision should not be expected for primates, which are often
opportunistic feeders. A relatively large amount of variation should be expected within a
species. Additionally, LMS examines a larger area of the tooth surface than the other
dental microwear methods. This results in a larger sample from which to gather data.
While dental microwear is acknowledged to be a dynamic trait, the morphological
structures that lead to dietary specialization are fixed. In the absence of those features,
such as crania and mandibles, dental microwear can serve as a proxy for a fixed trait
under the phylogenetic species concept. Other studies have shown that LMS can accurately predict the broad dietary specializations of specimens (Godfrey et al., 2004;
Semprebon et al., 2004). Using LMS as a proxy for a fixed trait in the fossil record provides a valuable new tool with which to examine complex taxonomic relationships.
As with most papers that address the issue of species designations in the Plio-
Pleistocene South African papionins (e.g. Freedman 1965, Groves 2000, Jablonski 2002,
Williams et al. 2007), the results presented here are somewhat equivocal at the species
level. The most significant insight into the species designations comes from the lack of 59
variation found in the extinct forms of Papio compared to the extant forms of Papio. In
light of the site differences, this is suggestive that the extinct forms of Papio do not have
enough variation in them for several species designations and should be collapsed into
one species with known site differences. However, this study examines dental microwear
exclusively and does not take into account any morphological differences.
Similarly, there was little variation found among the species of Parapapio, again
suggesting that if there are differences between the species they represent differences
other than those found from dietary signals. For example, those differences may be
temporal or they could be a result of misclassification of these three species that are
scaled versions of one another. It is possible that Parapapio is marked by more extreme sexual dimorphism than previously considered and that the scaled species of Parapapio are actually large males, small females, and moderately sized individuals.
The site analyses were similarly equivocal. There was little differentiation between sites except Makapansgat, where only Parapapio was found. However, the DFA was most successful at classifying specimens by site. The site level DFA resulted in the highest percentage points above chance, which is unexpected because species designations should be stronger than site differences. Since the difference seen at
Makapansgat is indicative of substantial time depth, it is likely that the site differences represent temporal differences.
The most revealing result was from the temporal (extinct versus extant) analysis and to a lesser extent the analysis of genera. Here, a clear turnover-pulse can be seen along with a change in diet. The evidence suggests that extinct forms were able to exploit the more wooded habitat while the extant forms adapted to the savanna. This is 60
particularly important in light of the hominid evolution that was occurring during this
time period. Jolly (2001) has argued that papionins are a good analogy for studying
hominid evolution due to their similar occurrence both in terms of geography and time.
This study further demonstrates that the papionins are good analogs for hominids by
showing the clear dietary shift that occurred during the Plio-Pleistocene climate change,
which may be useful for addressing some of the questions regarding climate change and
the emergence of the genus Homo (Bobe and Behrensmeyer, 2003). Other studies
(Carter, 2006) confirmed that southern African Australopithecus shows a diet that is indicative of a grassland ecology. As earlier hominid fossils are found in southern Africa a comparison of their dietary signals to the signals of older, east African hominid fossils as well as papionin specimens may demonstrate the adaptability of hominids to a grassland ecology.
Further research should continue to expand sample sizes, investigate site differences, elucidate the significance of those differences, make direct comparisons to hominids from southern Africa and expand the investigation to East Africa where a more precise chronology is available. Additionally, future studies should incorporate a more precise temporal analysis using dates based on the biochronologies of Delson (1984) and
Williams et al. (2007). As more studies address the evolution of the southern African papionins, a greater understanding of the paleoecology of hominid evolution may be obtained. 61
References
Albarede F, Balter V, Brage J, Blichert-Toft J, Telouk P, and Thackeray F (2006) U-Pb dating of enamel from the Swartkrans Cave hominid site (South Africa) by MC- ICP-MS. Geochimica et Cosmochimica Acta 70:A7.
Allison P (2001) Missing data. Thousand Oaks: Sage Publications.
Ambrose SH, and DeNiro MJ (1986) The isotopic ecology of East African Mammals. Oecologia 69:395-406.
Barlow C (2000) The ghosts of evolution: Nonsensical fruit, missing partners, and other ecological anachronisms. New York: Basic Books.
Benefit BR (1990) Diet, species diversity and distribution of African fossil baboons. Kroeber Anthropological Society Papers 71/72:77-93.
Benefit BR (2000) Old World monkey origins and diversification: An evolutionary study of diet and dentition. In PF Whitehead and C Jolly (eds.): Old World monkeys. Cambridge: Cambridge University Press, pp. 133-179.
Bobe R, and Behrensmeyer A (2003) The expansion of grassland ecosystems in Africa in relation to mammalian evolution and the origin of the genus Homo. Palaeogeography, Paleoclimatology, Paleoecology 207:399-420.
Brain CK (1981) The hunter or the hunted? An introduction to African cave taphonomy. Chicago: University of Chicago Press.
Broom R (1940) The South African Pleistocene cercopithecoid apes. Annals of the South African Museum 20:89-100.
Carter A, and Carter C (1999) Cultural representations of nonhuman primates. In P Dolhinow and A Fuentes (eds.): The nonhuman primates. Mountain View, CA: Mayfield. 62
Carter B (2006) Paleoecological reconstructions of the South African Plio-Pleistocene based on low-magnification dental microwear of fossil primates, M.A. Thesis, Georgia State University, Atlanta.
Covert HH, and Kay RF (1981) Dental microwear and diet: Implications for determining the feeding behaviors of extinct primates, with a comment on the dietary patterns of Sivapithecus. American Journal of Physical Anthropology 55:331-336.
Crompton AW, and Sita-Lumsden AG (1970) Functional significance of Therian molar pattern. Nature 227.
Daegling DJ, and Grine FE (1999) Terrestrial foraging and dental microwear in Papio ursinus. Primates 40:559-572.
Delson E (1975) Evolutionary history of the Cercopithecidae. Contributions to Primatology 5:167-217.
Delson E (1984) Cercopithecid biochronology of the African Plio-Pleistocene: Correlations among eastern and southern hominid-bearing localities. Courier Forschungsinstitut Seneckenberg 69:199-218 (as cited in Williams, Ackermann, et al., 2007).
deMenocal PB (1995) Plio-Pleistocene African climate. Science 270:53-59.
DeNiro MJ, and Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45:341-351.
Denton G (1999) Cenozoic climate change. In T Bromage and F Schrenk (eds.): African biogeography, climate change and human evolution. New York : Oxford University Press, pp. 94-114.
Disotell TR (1994) Generic level relationships of the Papionini (Cercopithecoidea). American Journal of Physical Anthropology 94:47-57.
Disotell TR (1996) The phylogeny of Old World monkeys. Evolutionary Anthropology 5:18-24. 63
Eaglen RH (1986) Morphometrics of the anterior dentition in strepsirhine primates. American Journal of Physical Anthropology 71:185-202.
El-Zaatari S, Grine FE, Teaford MF, and Smith HF (2005) Molar microwear and dietary reconstructions of fossil Cercopithecoidea from the Plio-Pleistocene deposits of South Africa. Journal of Human Evolution 49:180-205.
Freedman L (1957) The fossil Cercopithecoidea of South Africa. Annals of the South African Museum 23:121-262.
Freedman L (1960) Some new fossil Cercopithecoid specimens from Makapansgat, South Africa. Palaeontologia Africana 7:7-45.
Freedman L (1961) New Cercopithecoid fossils, including a new species, from Taung, Cape Province, South Africa. Annals of the South African Museum 46:1-14.
Freedman L (1965) Fossil and subfossil primates from the limestone deposits at Taung, Bolt's Farm and Witkrans, South Africa. Palaeontologia Africana 9:19-48.
Freedman L (1976) South African fossil Cercopithecoidea: A re-assessment including a description of new material from Makapansgat, Sterkfontein and Taung. Journal of Human Evolution 5:297-315.
Freedman L, and Stenhouse NS (1972) The Parapapio species of Sterkfontein, Transvaal, South Africa. Palaeontologia Africana 14:93-111.
Frost S, and Delson E (2002) Fossil Cercopithecidae from the Hadar Formation and surrounding areas of the Afar Depression, Ethiopia. Journal of Human Evolution 43:687-748.
Gear JHS (1926) A preliminary account of the baboon remains from Taungs. South African Journal of Science 23:731-747.
Godfrey LR, and Marks J (1991) The nature and origin of primate species. Yearbook of Physical Anthropology 34:39-68. 64
Godfrey LR, Semprebon GM, Jungers WL, Sutherland MR, Simons EL, and Solounias N (2004) Dental use wear in extinct lemurs: Evidence of diet and niche differentiation. Journal of Human Evolution 47:145-169.
Gordon KD (1982) A study of microwear on chimpanzee molars: Implications for dental microwear analysis. American Journal of Physical Anthropology 59:195-215.
Gordon KD (1983) Taphonomy of dental microwear: Can fossil microwear be studied productively? American Journal of Physical Anthropology 60 (suppl):200.
Gordon KD (1984) Hominoid dental mirowear: complications in the use of microwear analysis to detect diet. Journal of Dental Research 63:1043-1046.
Gordon KD (1988) A review of methodology and quantification in dental microwear analysis. Scanning Microscopy 2:1139-1147.
Gordon KD (2005) A study of microwear on chimpanzee molars: Implications for dental microwear analysis. American Journal of Physical Anthropology 59:195-215.
Gould SJ (1971) Geometric similarity in allometric growth: A contribution to the problem of scaling in the evolution of size. American Naturalist 105:113-136.
Greaves WS (1988) A functional consequence of an ossified mandibular symphysis. American Journal of Physical Anthropology 77:53-56.
Greaves WS (1993) Reply to Drs. Ravosa and Hylander. American Journal of Physical Anthropology 90:513-514.
Gregory WK (1922) The Origin and Evolution of Human Dentition. Baltimore: Williams and Wilkins.
Groves CP (2000) The phylogeny of the Cercopithecoidea. In PF Whitehead and C Jolly (eds.): Old World monkeys. Cambridge: Cambridge University Press, pp. 77-98.
Groves CP (2004) The what, why and how of primate taxonomy. International Journal of Primatology 25:1105-1126. 65
Groves CP, and Napier JR (1968) Dental dimensions and diet in australopithecines. Proceedings of the VIII International Congress for Anthropological and Ethnographic Sciences, pp. 273-276.
Harcourt AH (1998) Does primate socioecology need nonprimate socioecology? Evolutionary Anthropology 7:3-7.
Harcourt CS, and Nash LT (1986) Species differences in substrate use and diet between sympatric galagos in two Kenyan coastal forests. Primates 27:41-52.
Hiiemae KM, and Kay RF (1972) Trends in the evolution of primate mastication. Nature 240:486-487.
Hill T, and Lewicki P (2006) Statistics Methods and Applications. Tulsa, OK: StatSoft, Inc.
Jablonski NG (1994) New fossil cercopithecid remains from the Humpata Plateau, southern Angola. American Journal of Physical Anthropology 94:435-464.
Jablonski NG (2002) Fossil Old World monkeys: The late Neogene radiation. In WC Hartwig (ed.): The primate fossil record. Cambridge: Cambridge University Press, pp. 255-299.
Jolly C (1967) The evolution of baboons. In H Vagtbord (ed.): The baboon in medical research. Austin: University of Texas Press, pp. 427-457.
Jolly C (1970a) Hadropithecus: A lemuroid small object feeder. Man 5:619-626.
Jolly C (1970b) The seed eaters: A new model of hominid differentiation based on a baboon analog. Man 5:1-26.
Jolly C (2001) A proper study for mankind: Analogies from the papionin monkeys and their implications for human evolution. Yearbook of Physical Anthropology 44:177-204. 66
Jolly C (2006) Baboons, mandrills, and mangabeys: Afro-Papionin socioecology in a phylogenetic perspective. In C Campbell (ed.): Primates in Perspective. Oxford: Oxford University Press, pp. 240-251.
Jones TR (1937) A new fossil primate from Sterkfontein, Krugersdorp, Transvaal. South African Journal of Science 33:709-728.
Kay RF (1975) Allometry in early hominids. Science 189:63.
Kay RF (1978) Molar structure and diet in extant Cercopithecidae. In PM Butler and KA Joysey (eds.): Development, Function, and Evolution of Teeth. New York: Academic Press, pp. 309-339.
Kay RF (1981) The nut-crackers: A new theory of the adaptations of the Ramapithecinae. American Journal of Physical Anthropology 55:141-151.
Kay RF (1984) On the use of anatomical features to infer foraging behavior in extinct primates. In PS Rodman and JGH Cant (eds.): Adaptations for Foraging in Nonhuman Primates: Contributions to an Organismal Biology of Prosimians, Monkeys, and Apes. New York: Columbia University, pp. 21-53.
Kay RF, and Covert HH (1983) True grit: A microwear experiment. American Journal of Physical Anthropology 61:33-38.
Kay RF, and Covert HH (1984) Anatomy and behavior of extinct primates. In DJ Chivers and BA Wood (eds.): Food Aquisition and Processing in Primates. New York: Plenum Press, pp. 467-508.
Kay RF, and Hylander WL (1978) The dental structure of mammalian folivores with special reference to primates and Phalangeroidea (Marsupialia). In GG Montgomery (ed.): The Ecology of Arboreal Folivores. Washington, D. C. : Smithsonian Institution, pp. 173-191.
Kay RF, Schmitt D, Vinyard C, Perry J, Shigehara N, Takai M, and Egi N (2004) The paleobiology of Amphipithecidae, South Asian Late Eocene primates. Journal of Human Evolution 46:3-25. 67
Krebs JR, and Davies NB (1993) An introduction to behavioural ecology. Oxford: Blackwell Scientific Publications.
Laitman J (1986) Taung revisited: An examination of the past, present, and future of hominid evolution. Current Anthropology 27:78-80.
Leakey LSB, and Whitworth T (1958) Size differences not enough for distinct species: Notes on Simopithecus with a description of a new species from Olduvai. Coryndon Memorial Museum Occasional Papers 6:1-14.
Leakey MG, and Walker A (1997) Early hominid fossils from Africa. Scientific American 276:74-79.
Lee-Thorp JA, van der Merwe NJ, and Brain CK (1994) Diet of Australopithecus robustus at Swartkrans from stable carbon isotopis analysis. Journal of Human Evolution 27:361-372.
Lucas PW, and Luke DA (1984) Chewing it over: Basic principles of food breakdown. In DJ Chivers, BA Wood and A Bilsborough (eds.): Food Acquisition and Processing in Primates. New York: Plenum Press, pp. 173-203.
Lucas PW, Peters CR, and Arrandale SR (1994) Seed-breaking forces exerted by orangutans with their teeth in captivity and a new technique for estimating forces produced in the wild. American Journal of Physical Anthropology 94:365-378.
Lucas PW, and Teaford MF (1994) Functional morphology of colobine teeth. In AG Davies and JF Oates (eds.): Colobine Monkeys: Their Ecology, Behaviour and Evolution. Cambridge: Cambridge University Press, pp. 173-202.
Maas MC (1991) Enamel structure and microwear: An experimental study of the response of enamel to shearing forces. American Journal of Physical Anthropology 85:31-50.
Maas MC (1993) Enamel microstructure and molar wear in the greater galago, Otolemur crassicaudatus. American Journal of Physical Anthropology 92:217-233. 68
Maas MC (1994) A scanning electron-microscopic study of in vitro abrasion of mammalian tooth enamel under compressive loads. Archives of Oral Biology 39:1-11.
Maas MC, and O'Leary M (1996) Evolution of molar enamel microstructure in North American Notharctidae (primates). Journal of Human Evolution 31:293-310.
Maier W (1970) New fossil Cercopithecoidea from the lower Pleistocene cave deposits of the Makapansgat limeworks, South Africa. Palaeontologia Africana 13:69-107.
Maier W (1971) Two new skulls of Parapapio antiquus from Taung and a suggested phylogenetic arrangement of the genus Parapapio. Annals of the South African Museum 59:1-16.
McGrew WC, Baldwin PJ, and Tutin CEG (2005) Diet of wild chimpanzees (Pan troglodytes verus) at Mt. Assirik, Senegal: I. Composition. American Journal of Primatology 16:213-226.
McKee JK, Thackeray JF, and Berger LR (1995) Faunal assemblage seriation of southern Africa Pliocene and Pleistocene fossil deposits. American Journal of Physical Anthropology 96:235-250.
Meikle WE (1977) Molar wear stages in Theropithecus gelada. Kroeber Anthropological Society Papers 50:21-25.
Milton K (1981) Food choice and digestive strategies of two sympatric primate species. American Naturalist 117:496-505.
Moreno-Black G (1978) The use of scat samples in primate diet analysis. Primates 19:215-221.
Newman TK, Jolly C, and Rogers J (2003) Mitochondrial phylogeny and systematics of baboons (Papio). American Journal of Physical Anthropology 124:17-27.
Nystrom P, Phillips-Conroy JE, and Jolly C (2004) Dental microwear in anubis and hybrid baboons (Papio hamadryas, sensu lato) living in Awash National Park, Ethiopia. American Journal of Physical Anthropology 125:279-291. 69
Perez-Perez A, Lalueza C, and Turbon D (2005) Intraindividual and intragroup variability of buccal tooth striation pattern. American Journal of Physical Anthropology 94:175-187.
Phillips-Conroy JE, Jolly C, and Brett FL (1991) Characteristics of hamadryas-like male baboons living in anubis baboon troops in the Awash hybrid zone, Ethiopia. American Journal of Physical Anthropology 86:353-368.
Pilbeam D, and Gould SJ (1974) Size and scaling in human evolution. Science 188:892- 901.
Porter LM (2001) Dietary differences among sympatric Callitrichinae in Northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. International Journal of Primatology 22:961-992.
Potts R (1998) Environmental hypotheses of hominin evolution. Yearbook of Physical Anthropology 41:93-136.
Proctor D, and Hudson K (2006) Will the real Parapapio please stand up: Species differentiation in Parapapio using dental microwear: Paper Presented to the Georgia Academy of Sciences Annual Meeting. Lawrenceville, Georgia.
Reed KE (1997) Early hominid evolution and ecological change through the African Plio-Pleistocene. Journal of Human Evolution 32:289-322.
Reed KE (2002) The use of paleocommunity and taphonomic studies in reconstructing primate behavior. In MJ Plavcan, RF Kay, WL Jungers and CP van Schaik (eds.): Reconstructing Behavior in the Primate Fossil Record. New York: Kluwer Academic/Plenum Publishers, pp. 217-259.
Rensberger JM (1978) Scanning electron microscopy of wear and occlusal events in some small herbivores. Journal of Paleontology 47:512-528.
Robinson JT (1954) Prehominid dentition and hominid evolution. Evolution 8:324-334.
Rosenberger AL (1986) Platyrrhines, catarrhines and the anthropoid transition. In BA Wood, L Martin and P Andrews (eds.): Major Topics in Primate and Human Evolution. Cambridge: Cambridge University Press, pp. 66-88. 70
Samuels A, and Altmann J (1986) Immigration of a Papio anubis male into a group of Papio cynocephalus baboons and evidence for an anubis-cynocephalus hybrid zone in Amboseli, Kenya. International Journal of Primatology 7:131-138.
Scholz M, Bachmann L, Nicholson G, BAchmann J, Giddings I, Ruschoff-Thale B, Czarnetzki A, and Pusch C (2000) Genomic differentiation of Neanderthals and anatomically modern man allows a fossil-DNA-based classification of morphologically indistinguishable hominid bones. The American Journal of Human Genetics 66:1927-1932.
Schrader JL (1986) A medieval bestiary. The Metropolitan Museum of Art Bulliten 44:12-55.
Scott R, Ungar PS, Bergstrom TS, Brown CA, Grine FE, Teaford MF, and Walker A (2005) Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436:693-695.
Semprebon GM, Godfrey LR, Solounias N, Sutherland MR, and Jungers WL (2004) Can low-magnification stereomicroscopy reveal diet? Journal of Human Evolution 47:115-144.
Sillen A (1992) Strontium-calcium ratios (Sr/Ca) of Australopithecus robustus and associated fauna from Swartkrans. Journal of Human Evolution 23:495-516.
Simons CL, and Delson E (1978) Cercopithecidae and Parapithecidae. In VJ Maglio and HBS Cooke (eds.): Evolution of African mammals. Cambridge: Harvard University Press, pp. 100-119.
Simons EL (1976) The nature of the transition in the dental mechanism from pongids to hominids. Journal of Human Evolution 5:511-528.
Simons EL, and Pilbeam D (1972) Hominoid paleoprimatology. In R Tuttle (ed.): The Functional and Evolutionary Biology of Primates. New York: Aldine-Atherion, pp. 36-62.
Simpson GG (1933) Paleobiology of jurassic mammals. Paleobiology 5:127-158. 71
Szalay FS, and Delson E (1979) Evolutionary history of the primates. New York: Academic Press.
Teaford MF (1982) Differences in molar wear gradient between juvenile macaques and langurs. American Journal of Physical Anthropology 57:323-330.
Teaford MF (1985) Molar microwear and diet in the genus Cebus. American Journal of Physical Anthropology 66:363-370.
Teaford MF (1988) A review of dental microwear and diet in modern mammals. Scanning Microscopy 2:1149-1166.
Teaford MF (1993) Dental microwear and diet in extant and extinct Theropithecus: a preliminary analysis. In NG Jablonski (ed.): Theropithecus: The rise and fall of a primate genus. Cambridge: Cambridge University Press, pp. 331-349.
Teaford MF (1994) Dental Microwear and dental function. Evolutionary Anthropology 3:17-30.
Teaford MF, and Leakey MG (1992) Dental microwear and diet in Plio-Pleistocene cercopithecoids from Kenya. American Journal of Physical Anthropology 14 [suppl]:160 [abstract].
Teaford MF, and Robinson JA (1989) Seasonal or ecological differences in diet and molar microwear in Cebus nigrivittatus. American Journal of Physical Anthropology 80:391-401.
Teaford MF, and Walker A (1984) Quantitative differences in dental microwear between primate species with different diets and a comment on the presumed diet of Sivapithecus. American Journal of Physical Anthropology 64:191-200.
Tutin CEG, and Fernandez M (2005) Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lope Reserve, Gabon. American Journal of Primatology 30:195-211.
Ungar PS (1996) Dental microwear of European Miocene catarrhines: Evidence for diets and tooth use. Journal of Human Evolution 31:335-366. 72
Ungar PS (1998) Dental allometry, morphology, and wear as evidence for diet in fossil primates. Evolutionary Anthropology 6:205-217.
Ungar PS (1999) Relationship of incisor size to diet and anterior tooth use in sympatric Sumatran anthropoids. American Journal of Primatology 38:145-156.
Ungar PS (2002) Reconstructing the Diets of Fossil Primates. In MJ Plavcan, RF Kay, WL Jungers and CP van Schaik (eds.): Reconstructing Behavior in the Primate Fossil Record. New York: Kluwer Academic/Plenum Publishers, pp. 261-296.
Ungar PS, Brown CA, Bergstrom TS, and Walker A (2003) Quantification of dental microwear by tandem scanning confocal microscopy and scale-sensitive fractal analyses. Scanning Microscopy 25:185-193.
Ungar PS, Teaford MF, Glander KE, and Pastor RF (1995) Dust accumulation in the canopy: A potential cause of dental microwear in primates. American Journal of Physical Anthropology 97:93-99.
Vrba ES (1975) Some evidence of chronology and palaeoecology of Sterkfontein, Swartkrans and Kromdraai from the fossil bovidae. Nature 254:301-304.
Vrba ES (1983) Macroevolutionary trends: New perspectives on the roles of adaptation and incidental effect. Science 221:387-389.
Vrba ES (1993) Turnover-pulses, the red queen and related topics. American Journal of Science 293:418-452.
Vrba ES (1996) Climate, Heterochrony and Human Evolution. Journal of Anthropological Research 52:1-28.
Walker A, Hoeck HN, and Perez L (1978) Microwear of mammalian teeth as an indicator of diet. Science 201:808-810.
Walker PL (1976) Wear striations on the incisors of cercopithecoid monkeys as an index of diet and habitat preference. American Journal of Physical Anthropology 45:299-308. 73
Williams F, Ackermann R, and Leigh S (2007) Inferring Plio-Pleistocene southern African biochronology from facial affinities in Parapapio and other fossil papionins. American Journal of Physical Anthropology 132:163-174.
Williams F, Clymer G, and Proctor D (2006) Is Papio robinsoni or Papio angusticeps a better dietary ancestor for Papio ursinus? American Journal of Physical Anthropology 129:188.
Williamson EA, Tutin CEG, Rogers ME, and Fernandez M (2005) Composition of the diet of lowland gorillas at Lope in Gabon. American Journal of Primatology 21:265-277.
Wolpoff MH (1973) Posterior tooth size, body size, and diet in South African gracile australopithecines. American Journal of Physical Anthropology 39:375-393.
Zachos J, Pagani M, Sloan L, Thomas E, and Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686-693.
74
Appendix
Specimens by Species
Specimen Species Time Site Museum CO102 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO104 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO106c P. angusticeps Extinct Cooper's Cave Transvaal Museum CO107a P. angusticeps Extinct Cooper's Cave Transvaal Museum CO115/103 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO117 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO118 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO134a P. angusticeps Extinct Cooper's Cave Transvaal Museum CO134b P. angusticeps Extinct Cooper's Cave Transvaal Museum CO134d P. angusticeps Extinct Cooper's Cave Transvaal Museum CO135a P. angusticeps Extinct Cooper's Cave Transvaal Museum CO135a2 P. angusticeps Extinct Cooper's Cave Transvaal Museum KA 151 P. angusticeps Extinct Kromdraai Transvaal Museum KA 156 P. angusticeps Extinct Kromdraai Transvaal Museum KA 166A P. angusticeps Extinct Kromdraai Transvaal Museum KA 194 P. angusticeps Extinct Kromdraai Transvaal Museum MCZ 15378 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 17342 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 17342 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 21160 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 21161 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 23091 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 23803 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 23805 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 26472 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 26473 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 29728 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 29786 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 31619 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 8304 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 23082 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 44276 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 169 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 5008 P. anubis Extant East-Central Africa Museum Comparative Zoology TP 10 P. izodi Extinct Taung South African Museum SAM 11728 P. izodi Extinct Taung South African Museum SAM 11730 P. izodi Extinct Taung South African Museum SAM 5356 P. izodi Extinct Taung Witwatersrand University Medical School TP 11 P. izodi Extinct Taung Witwatersrand University Medical School Institut Royal des Sciences Naturelles IRSNB 10616 P. kindae Extant Central Africa Belgique
75
Institut Royal des Sciences Naturelles IRSNB 10618 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10619 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10624 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10625 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10627 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10628 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10629 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10632 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10633 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10634 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10635 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10636 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10639 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10641 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10642 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 12863 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 7885 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 807 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 8531 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 9102 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10626 P. kindae Extant Central Africa Belgique BF 38 P. robinsoni Extinct Bolt's Farm Witwatersrand University Medical School SK 14083 P. robinsoni Extinct Swartkrans Transvaal Museum SK 406 P. robinsoni Extinct Swartkrans Transvaal Museum SK 407 P. robinsoni Extinct Swartkrans Transvaal Museum SK 408 P. robinsoni Extinct Swartkrans Transvaal Museum SK 416 P. robinsoni Extinct Swartkrans Transvaal Museum SK 417 P. robinsoni Extinct Swartkrans Transvaal Museum SK 421 P. robinsoni Extinct Swartkrans Transvaal Museum SK 423 P. robinsoni Extinct Swartkrans Transvaal Museum SK 436 P. robinsoni Extinct Swartkrans Transvaal Museum SK 445 P. robinsoni Extinct Swartkrans Transvaal Museum SK 458 P. robinsoni Extinct Swartkrans Transvaal Museum SK 536 P. robinsoni Extinct Swartkrans Transvaal Museum SK 549 P. robinsoni Extinct Swartkrans Transvaal Museum 76
SK 557 P. robinsoni Extinct Swartkrans Transvaal Museum SK 558 P. robinsoni Extinct Swartkrans Transvaal Museum SK 560 P. robinsoni Extinct Swartkrans Transvaal Museum SK 565 P. robinsoni Extinct Swartkrans Transvaal Museum SK 566 P. robinsoni Extinct Swartkrans Transvaal Museum SK 571B P. robinsoni Extinct Swartkrans Transvaal Museum SK 602 P. robinsoni Extinct Swartkrans Transvaal Museum ZM 33672 P. ursinus Extant South Africa South African Museum ZM 35953 P. ursinus Extant South Africa South African Museum ZM 36895 P. ursinus Extant South Africa South African Museum ZM 37165 P. ursinus Extant South Africa South African Museum ZM 37273A P. ursinus Extant South Africa South African Museum ZM 37273B P. ursinus Extant South Africa South African Museum ZM 37273C P. ursinus Extant South Africa South African Museum ZM 37274 P. ursinus Extant South Africa South African Museum ZM 37675 P. ursinus Extant South Africa South African Museum ZM 37676 P. ursinus Extant South Africa South African Museum ZM 37678 P. ursinus Extant South Africa South African Museum ZM 38318 P. ursinus Extant South Africa South African Museum ZM 38323 P. ursinus Extant South Africa South African Museum ZM 38335 P. ursinus Extant South Africa South African Museum ZM 38340 P. ursinus Extant South Africa South African Museum ZM 38343 P. ursinus Extant South Africa South African Museum ZM 38354 P. ursinus Extant South Africa South African Museum ZM 38355 P. ursinus Extant South Africa South African Museum ZM 38361 P. ursinus Extant South Africa South African Museum ZM 38363 P. ursinus Extant South Africa South African Museum ZM 38364 P. ursinus Extant South Africa South African Museum ZM 38365 P. ursinus Extant South Africa South African Museum ZM 38366 P. ursinus Extant South Africa South African Museum ZM 38368 P. ursinus Extant South Africa South African Museum ZM 38369 P. ursinus Extant South Africa South African Museum ZM 38371 P. ursinus Extant South Africa South African Museum ZM 38373 P. ursinus Extant South Africa South African Museum ZM 38376 P. ursinus Extant South Africa South African Museum ZM 38380 P. ursinus Extant South Africa South African Museum ZM 40415 P. ursinus Extant South Africa South African Museum KA 157 Pp. (sp) Extinct Kromdraai Transvaal Museum KA 162 Pp. (sp) Extinct Kromdraai Transvaal Museum TP 13 Pp. (sp) Extinct Taung Transvaal Museum TP 8 Pp. (sp) Extinct Taung Transvaal Museum T 17 Pp. broomi Extinct Taung Witwatersrand University Medical School M 3056 Pp. broomi Extinct Makapansgat Witwatersrand University Medical School MP 118 Pp. broomi Extinct Makapansgat Witwatersrand University Medical School MP 151 Pp. broomi Extinct Makapansgat Transvaal Museum STS 413B Pp. broomi Extinct Sterkfontein Transvaal Museum STS 1237 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 251 Pp. broomi Extinct Sterkfontein Transvaal Museum 77
STS 256 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 262 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 268 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 274 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 280 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 305 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 325 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 343 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 354 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 362 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 368A Pp. broomi Extinct Sterkfontein Transvaal Museum STS 371 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 374A Pp. broomi Extinct Sterkfontein Transvaal Museum STS 378A Pp. broomi Extinct Sterkfontein Transvaal Museum STS 398A Pp. broomi Extinct Sterkfontein Transvaal Museum STS 414B Pp. broomi Extinct Sterkfontein Transvaal Museum STS 562 Pp. broomi Extinct Sterkfontein Transvaal Museum STS unnumb Pp. broomi Extinct Sterkfontein Transvaal Museum KA 160 Pp. jonesi Extinct Kromdraai Transvaal Museum SK 412 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 414 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 418 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 433 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 437 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 462 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 537A Pp. jonesi Extinct Swartkrans Transvaal Museum SK 579 Pp. jonesi Extinct Swartkrans Transvaal Museum STS 250 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 287 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 306 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 329 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 333 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 340 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 355 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 367 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 372A Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 381 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 390 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS unnumb max. Pp. jonesi Extinct Sterkfontein Transvaal Museum STS unnumb Pp. jonesi Extinct Sterkfontein Transvaal Museum SK 550 Pp. whitei Extinct Swartkrans Witwatersrand University Medical School TP 9 Pp. whitei Extinct Taung Witwatersrand University Medical School BF 43 Pp. whitei Extinct Bolt's Farm Witwatersrand University Medical School MP 117 Pp. whitei Extinct Makapansgat Witwatersrand University Medical School MP 221 Pp. whitei Extinct Makapansgat Witwatersrand University Medical School MP 223 Pp. whitei Extinct Makapansgat Witwatersrand University Medical School MP 224 Pp. whitei Extinct Makapansgat Witwatersrand University Medical School 78
MP 239 Pp. whitei Extinct Makapansgat Transvaal Museum STS 253 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 259 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 263 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 266 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 303 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 323 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 342 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 352 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 353 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 359 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 370A Pp. whitei Extinct Sterkfontein Transvaal Museum STS 370B Pp. whitei Extinct Sterkfontein Transvaal Museum STS 414A Pp. whitei Extinct Sterkfontein Transvaal Museum STS 563 Pp. whitei Extinct Sterkfontein Transvaal Museum STS unnumbered Pp. whitei Extinct Sterkfontein Witwatersrand University Medical School TP 12 Pp. whitei Extinct Taung Witwatersrand University Medical School TP 89-154 Pp. whitei Extinct Taung Witwatersrand University Medical School
79
Specimens by Site
Specimen Species Time Site Museum BF 38 P. robinsoni Extinct Bolt's Farm Witwatersrand University Medical School BF 43 Pp. whitei Extinct Bolt's Farm Witwatersrand University Medical School Institut Royal des Sciences Naturelles IRSNB 10616 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10618 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10619 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10624 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10625 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10627 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10628 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10629 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10632 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10633 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10634 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10635 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10636 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10639 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10641 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10642 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 12863 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 7885 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 807 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 8531 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 9102 P. kindae Extant Central Africa Belgique Institut Royal des Sciences Naturelles IRSNB 10626 P. kindae Extant Central Africa Belgique CO102 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO104 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO106c P. angusticeps Extinct Cooper's Cave Transvaal Museum CO107a P. angusticeps Extinct Cooper's Cave Transvaal Museum CO115/103 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO117 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO118 P. angusticeps Extinct Cooper's Cave Transvaal Museum CO134a P. angusticeps Extinct Cooper's Cave Transvaal Museum 80
CO134b P. angusticeps Extinct Cooper's Cave Transvaal Museum CO134d P. angusticeps Extinct Cooper's Cave Transvaal Museum CO135a P. angusticeps Extinct Cooper's Cave Transvaal Museum CO135a2 P. angusticeps Extinct Cooper's Cave Transvaal Museum MCZ 15378 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 17342 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 17342 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 21160 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 21161 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 23091 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 23803 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 23805 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 26472 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 26473 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 29728 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 29786 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 31619 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 8304 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 23082 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 44276 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 169 P. anubis Extant East-Central Africa Museum Comparative Zoology MCZ 5008 P. anubis Extant East-Central Africa Museum Comparative Zoology KA 151 P. angusticeps Extinct Kromdraai Transvaal Museum KA 156 P. angusticeps Extinct Kromdraai Transvaal Museum KA 166A P. angusticeps Extinct Kromdraai Transvaal Museum KA 194 P. angusticeps Extinct Kromdraai Transvaal Museum KA 157 Pp. (sp) Extinct Kromdraai Transvaal Museum KA 162 Pp. (sp) Extinct Kromdraai Transvaal Museum KA 160 Pp. jonesi Extinct Kromdraai Transvaal Museum M 3056 Pp. broomi Extinct Makapansgat Witwatersrand University Medical School MP 118 Pp. broomi Extinct Makapansgat Witwatersrand University Medical School MP 151 Pp. broomi Extinct Makapansgat Transvaal Museum MP 117 Pp. whitei Extinct Makapansgat Witwatersrand University Medical School MP 221 Pp. whitei Extinct Makapansgat Witwatersrand University Medical School MP 223 Pp. whitei Extinct Makapansgat Witwatersrand University Medical School MP 224 Pp. whitei Extinct Makapansgat Witwatersrand University Medical School MP 239 Pp. whitei Extinct Makapansgat Transvaal Museum ZM 33672 P. ursinus Extant South Africa South African Museum ZM 35953 P. ursinus Extant South Africa South African Museum ZM 36895 P. ursinus Extant South Africa South African Museum ZM 37165 P. ursinus Extant South Africa South African Museum ZM 37273A P. ursinus Extant South Africa South African Museum ZM 37273B P. ursinus Extant South Africa South African Museum ZM 37273C P. ursinus Extant South Africa South African Museum ZM 37274 P. ursinus Extant South Africa South African Museum ZM 37675 P. ursinus Extant South Africa South African Museum ZM 37676 P. ursinus Extant South Africa South African Museum ZM 37678 P. ursinus Extant South Africa South African Museum 81
ZM 38318 P. ursinus Extant South Africa South African Museum ZM 38323 P. ursinus Extant South Africa South African Museum ZM 38335 P. ursinus Extant South Africa South African Museum ZM 38340 P. ursinus Extant South Africa South African Museum ZM 38343 P. ursinus Extant South Africa South African Museum ZM 38354 P. ursinus Extant South Africa South African Museum ZM 38355 P. ursinus Extant South Africa South African Museum ZM 38361 P. ursinus Extant South Africa South African Museum ZM 38363 P. ursinus Extant South Africa South African Museum ZM 38364 P. ursinus Extant South Africa South African Museum ZM 38365 P. ursinus Extant South Africa South African Museum ZM 38366 P. ursinus Extant South Africa South African Museum ZM 38368 P. ursinus Extant South Africa South African Museum ZM 38369 P. ursinus Extant South Africa South African Museum ZM 38371 P. ursinus Extant South Africa South African Museum ZM 38373 P. ursinus Extant South Africa South African Museum ZM 38376 P. ursinus Extant South Africa South African Museum ZM 38380 P. ursinus Extant South Africa South African Museum ZM 40415 P. ursinus Extant South Africa South African Museum STS 413B Pp. broomi Extinct Sterkfontein Transvaal Museum STS 1237 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 251 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 256 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 262 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 268 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 274 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 280 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 305 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 325 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 343 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 354 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 362 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 368A Pp. broomi Extinct Sterkfontein Transvaal Museum STS 371 Pp. broomi Extinct Sterkfontein Transvaal Museum STS 374A Pp. broomi Extinct Sterkfontein Transvaal Museum STS 378A Pp. broomi Extinct Sterkfontein Transvaal Museum STS 398A Pp. broomi Extinct Sterkfontein Transvaal Museum STS 414B Pp. broomi Extinct Sterkfontein Transvaal Museum STS 562 Pp. broomi Extinct Sterkfontein Transvaal Museum STS unnumbered Pp. broomi Extinct Sterkfontein Transvaal Museum STS 250 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 287 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 306 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 329 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 333 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 340 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 355 Pp. jonesi Extinct Sterkfontein Transvaal Museum 82
STS 367 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 372A Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 381 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 390 Pp. jonesi Extinct Sterkfontein Transvaal Museum STS unnumb max. Pp. jonesi Extinct Sterkfontein Transvaal Museum STS unnumbered Pp. jonesi Extinct Sterkfontein Transvaal Museum STS 253 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 259 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 263 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 266 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 303 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 323 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 342 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 352 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 353 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 359 Pp. whitei Extinct Sterkfontein Transvaal Museum STS 370A Pp. whitei Extinct Sterkfontein Transvaal Museum STS 370B Pp. whitei Extinct Sterkfontein Transvaal Museum STS 414A Pp. whitei Extinct Sterkfontein Transvaal Museum STS 563 Pp. whitei Extinct Sterkfontein Transvaal Museum STS unnumbered Pp. whitei Extinct Sterkfontein Witwatersrand University Medical School SK 14083 P. robinsoni Extinct Swartkrans Transvaal Museum SK 406 P. robinsoni Extinct Swartkrans Transvaal Museum SK 407 P. robinsoni Extinct Swartkrans Transvaal Museum SK 408 P. robinsoni Extinct Swartkrans Transvaal Museum SK 416 P. robinsoni Extinct Swartkrans Transvaal Museum SK 417 P. robinsoni Extinct Swartkrans Transvaal Museum SK 421 P. robinsoni Extinct Swartkrans Transvaal Museum SK 423 P. robinsoni Extinct Swartkrans Transvaal Museum SK 436 P. robinsoni Extinct Swartkrans Transvaal Museum SK 445 P. robinsoni Extinct Swartkrans Transvaal Museum SK 458 P. robinsoni Extinct Swartkrans Transvaal Museum SK 536 P. robinsoni Extinct Swartkrans Transvaal Museum SK 549 P. robinsoni Extinct Swartkrans Transvaal Museum SK 557 P. robinsoni Extinct Swartkrans Transvaal Museum SK 558 P. robinsoni Extinct Swartkrans Transvaal Museum SK 560 P. robinsoni Extinct Swartkrans Transvaal Museum SK 565 P. robinsoni Extinct Swartkrans Transvaal Museum SK 566 P. robinsoni Extinct Swartkrans Transvaal Museum SK 571B P. robinsoni Extinct Swartkrans Transvaal Museum SK 602 P. robinsoni Extinct Swartkrans Transvaal Museum SK 412 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 414 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 418 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 433 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 437 Pp. jonesi Extinct Swartkrans Transvaal Museum 83
SK 462 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 537A Pp. jonesi Extinct Swartkrans Transvaal Museum SK 579 Pp. jonesi Extinct Swartkrans Transvaal Museum SK 550 Pp. whitei Extinct Swartkrans Witwatersrand University Medical School TP 10 P. izodi Extinct Taung South African Museum SAM 11728 P. izodi Extinct Taung South African Museum SAM 11730 P. izodi Extinct Taung South African Museum SAM 5356 P. izodi Extinct Taung Witwatersrand University Medical School TP 11 P. izodi Extinct Taung Witwatersrand University Medical School TP 13 Pp. (sp) Extinct Taung Transvaal Museum TP 8 Pp. (sp) Extinct Taung Transvaal Museum T 17 Pp. broomi Extinct Taung Witwatersrand University Medical School TP 9 Pp. whitei Extinct Taung Witwatersrand University Medical School TP 12 Pp. whitei Extinct Taung Witwatersrand University Medical School TP 89-154 Pp. whitei Extinct Taung Witwatersrand University Medical School